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New Insights into mtDNA, mitochondrial proteins, aging, and metabolic control

Larry H. Bernstein, MD, FCAP, Curator

LPBI

 

Newly discovered proteins may protect against age-related illnesses  

The proteins could play a key role in the aging process and the onset of diseases linked to older age

BY Beth Newcomb   APRIL 13, 2016

http://news.usc.edu/98412/newly-discovered-proteins-may-protect-against-agings-illnesses/

http://news.usc.edu/files/2016/04/20160208_PinchasCohen_web-824×549.jpg

Pinchas Cohen led a team that identified tiny proteins that appear to play a role in controlling how the body ages. (Photo/Beth Newcomb)

A group of six newly discovered proteins may help to divulge secrets of how we age, potentially unlocking insights into diabetes, Alzheimer’s, cancer and other aging-related diseases.

The tiny proteins appear to play several big roles in our bodies’ cells, from decreasing the amount of damaging free radicals and controlling the rate at which cells die to boosting metabolism and helping tissues throughout the body respond better to insulin. The naturally occurring amounts of each protein decrease with age, leading researchers to believe that they play an important role in the aging process and the onset of diseases linked to older age.

The research team led by Pinchas Cohen, dean of the USC Davis School of Gerontology, identified the tiny proteins for the first time and observed their surprising origin from organelles in the cell called mitochondria and their game-changing roles in metabolism and cell survival. This latest finding builds upon prior research by Cohen and his team that uncovered two significant proteins, humanin and MOTS-c, hormones that appear to have significant roles in metabolism and diseases of aging.

Unlike most other proteins, humanin and MOTS-c are encoded in mitochondria, the structure within cells that produces energy from food, instead of in the cell’s nucleus where most genes are contained.

Key functions

Mitochondria have their own small collection of genes, which were once thought to play only minor roles within cells but now appear to have important functions throughout the body. Cohen’s team used computer analysis to see if the part of the mitochondrial genome that provides the code for humanin was coding for other proteins as well. The analysis uncovered the genes for six new proteins, which were dubbed small humanin-like peptides, or SHLPs, 1 through 6 (the name of this hardworking group of proteins is appropriately pronounced “schlep”).

After identifying the six SHLPs and successfully developing antibodies to test for several of them, the team examined both mouse tissues and human cells to determine their abundance in different organs as well as their functions. The proteins were distributed quite differently among organs, which suggests that the proteins have varying functions based on where they are in the body.

Of particular interest is SHLP 2, Cohen said. The protein appears to have profound insulin-sensitizing, anti-diabetic effects as well as potent neuro-protective activity that may emerge as a strategy to combat Alzheimer’s disease. He added that SHLP 6 is also intriguing, with a unique ability to promote cancer cell death and thus potentially target malignant diseases.

“Together with the previously identified mitochondrial peptides, the newly recognized SHLP family expands the understanding of the mitochondria as an intracellular signaling organelle that communicates with the rest of the body to regulate metabolism and cell fate,” Cohen said. “The findings are an important advance that will be ripe for rapid translation into drug development for diseases of aging.”

The study first appeared online in the journal Aging on April 10. Cohen’s research team included collaborators from the Albert Einstein College of Medicine; the findings have been licensed to the biotechnology company CohBar for possible drug development.

The research was supported by a Glenn Foundation Award and National Institutes of Health grants to Cohen (1P01AG034906, 1R01AG 034430, 1R01GM 090311, 1R01ES 020812) and an Ellison/AFAR postdoctoral fellowship to Kelvin Yen. Study authors Laura Cobb, Changhan Lee, Nir Barzilai and Pinchas Cohen are consultants and stockholders of CohBar Inc.

Feature: The man who wants to beat back aging

By Stephen S. Hall Sep. 16, 201

Nir Barzilai hopes to persuade FDA to bless the proposed anti-aging trial, which is unconventional in its goals and design.
http://www.sciencemag.org/news/2015/09/feature-man-who-wants-beat-back-aging

On a blazingly hot morning this past June, a half-dozen scientists convened in a hotel conference room in suburban Maryland for the dress rehearsal of what they saw as a landmark event in the history of aging research. In a few hours, the group would meet with officials at the U.S. Food and Drug Administration (FDA), a few kilometers away, to pitch an unprecedented clinical trial—nothing less than the first test of a drug to specifically target the process of human aging.

“We think this is a groundbreaking, perhaps paradigm-shifting trial,” said Steven Austad, chairman of biology at the University of Alabama, Birmingham, and scientific director of the American Federation for Aging Research (AFAR). After Austad’s brief introductory remarks, a scientist named Nir Barzilai tuned up his PowerPoint and launched into a practice run of the main presentation.

Barzilai is a former Israeli army medical officer and head of a well-known study of centenarians based at the Albert Einstein College of Medicine in the Bronx, New York. To anyone who has seen the ebullient scientist in his natural laboratory habitat, often in a short-sleeved shirt and always cracking jokes, he looked uncharacteristically kempt in a blue blazer and dress khakis. But his practice run kept hitting a historical speed bump. He had barely begun to explain the rationale for the trial when he mentioned, in passing, “lots of unproven, untested treatments under the category of anti-aging.” His colleagues pounced.

“Nir,” interrupted S. Jay Olshansky, a biodemographer of aging from the University of Illinois, Chicago. The phrase “anti-aging … has an association that is negative.”

“I wouldn’t dignify them by calling them ‘treatments,’” added Michael Pollak, director of cancer prevention at McGill University in Montreal, Canada. “They’re products.”

Barzilai, a 59-year-old with a boyish mop of gray hair, wore a contrite grin. “We know the FDA is concerned about this,” he conceded, and deleted the offensive phrase.

Then he proceeded to lay out the details of an ambitious clinical trial. The group—academics all—wanted to conduct a double-blind study of roughly 3000 elderly people; half would get a placebo and half would get an old (indeed, ancient) drug for type 2 diabetes called metformin, which has been shown to modify aging in some animal studies. Because there is still no accepted biomarker for aging, the drug’s success would be judged by an unusual standard—whether it could delay the development of several diseases whose incidence increases dramatically with age: cardiovascular disease, cancer, and cognitive decline, along with mortality. When it comes to these diseases, Barzilai is fond of saying, “aging is a bigger risk factor than all of the other factors combined.”

But the phrase “anti-aging” kept creeping into the rehearsal, and critics kept jumping in. “Okay,” Barzilai said with a laugh when it came up again. “Third time, the death penalty.”

The group’s paranoia about the term “anti-aging” captured both the audacity of the proposed trial and the cultural challenge of venturing into medical territory historically associated with charlatans and quacks. The metformin initiative, which Barzilai is generally credited with spearheading, is unusual by almost any standard of drug development. The people pushing for the trial are all academics, none from industry (although Barzilai is co-founder of a biotech company, CohBar Inc., that is working to develop drugs targeting age-related diseases). The trial would be sponsored by the nonprofit AFAR, not a pharmaceutical company. No one stood to make money if the drug worked, the scientists all claimed; indeed, metformin is not only generic, costing just a few cents a dose, but belongs to a class of drugs that has been part of the human apothecary for 500 years. Patient safety was unlikely to be an issue; millions of diabetics have taken metformin since the 1960s, and its generally mild side effects are well-known.

Finally, the metformin group insisted they didn’t need a cent of federal money to proceed (although they do intend to ask for some). Nor did they need formal approval from FDA to proceed. But they very much wanted the agency’s blessing. By recognizing the merit of such a trial, Barzilai believes,  FDA would make aging itself a legitimate target for drug development.

By the time the scientists were done, the rehearsal—which was being filmed for a television documentary—had the feel of a pep rally. They spoke with unguarded optimism. “What we’re talking about here,” Olshansky said, “is a fundamental sea change in how we look at aging and disease.” To Austad, it is “the key, potentially, to saving the health care system.”

As the group piled into a van for the drive to FDA headquarters, there was more talk about setting precedents and opening doors. So it was a little disconcerting when Austad led the delegation up to the main entrance of FDA—and couldn’t get the door open.   ……

Mitochondrial Peptides Found in a Preclinical Study Seen to Control Cell Metabolism

APRIL 13, 2016 BY MAGDALENA KEGEL  IN NEWS.
http://mitochondrialdiseasenews.com/2016/04/13/newly-discovered-mitochondrial-factors-might-give-insights-into-aging/

 

CohBar, a developer of mitochondria-based therapeutics, announced that preclinical research by its academic collaborators has found small humanin-like peptides (SHLPs) that can control metabolism and cell survival. The findings have implications for age-related diseases such as Alzheimer’s and cancer.

The study, “Naturally Occurring Mitochondrial-derived Peptides are Age-dependent Regulators of Apoptosis, Insulin Sensitivity, and Inflammatory Markers,” was the result of a joint effort between researchers at the University of Southern California (USC) and theInstitute for Aging Research at the Albert Einstein College of Medicine of Yeshiva University. The study was published in the journal Aging.

Researchers discovered the SHLPs by examining the genome of mitochondria with the help of a bioinformatics approach, which identified six peptides. The team then verified the presence of the factors and explored their function in laboratory animals.

CohBar, who have the exclusive license to develop SHLPs into therapeutics, works closely with its academic partners to explore the peptides in preclinical models.

While it was previously believed that mitochondria only have 37 genes, research has revealed that the mitochondrial genome is far more versatile, potentially harboring a multitude of new genes, which can encode peptides acting as cellular signaling factors. The peptides, it has turned out, have shown neuroprotective and anti-inflammatory effects, and act to protect cells in disease-modifying ways in preclinical models of aging.

CohBar’s goal is to bring these peptides to the market as therapies for age-related diseases, such as obesity, type 2 diabetes, cancer, atherosclerosis and neurodegenerative disorders.

“Together with the previously described mitochondrial-derived peptides humanin and MOTS-c, the SHLP family expands our understanding of the role that these peptides play in intracellular signaling throughout the body to regulate both metabolism and cell survival,” Pinchas Cohen, dean of the USC Leonard Davis School of Gerontology, founder and director of CohBar, and the study’s senior author, said in a press release. “These findings further illustrate the enormous potential that mitochondria-based therapeutics could have on treating age-associated diseases like Alzheimer’s and cancer.”

“The pre-clinical evidence continues to confirm that these peptides represent a new class of naturally occurring metabolic regulators,” added Simon Allen, CohBar’s CEO. “They form the foundation of our pipeline of first-in-class treatments for age-related diseases, and we are committed to rapidly advancing them through pre-clinical and clinical activities as we move forward.”

Naturally occurring mitochondrial-derived peptides are age-dependent regulators of apoptosis, insulin sensitivity, and inflammatory markers

Laura J. Cobb1,5, Changhan Lee2, Jialin Xiao2, Kelvin Yen2, Richard G. Wong2, Hiromi K. Nakamura1, ….., Derek M. Huffman4, Junxiang Wan2, Radhika Muzumdar3, Nir Barzilai4 , and Pinchas Cohen2
http://www.impactaging.com/papers/v8/n4/full/100943.html

Mitochondria are key players in aging and in the pathogenesis of age-related diseases. Recent mitochondrial transcriptome analyses revealed the existence of multiple small mRNAs transcribed from mitochondrial DNA (mtDNA). Humanin (HN), a peptide encoded in the mtDNA 16S ribosomal RNA region, is a neuroprotective factor. An in silico search revealed six additional peptides in the same region of mtDNA as humanin; we named these peptides small humanin-like peptides (SHLPs). We identified the functional roles for these peptides and the potential mechanisms of action. The SHLPs differed in their ability to regulate cell viability in vitro. We focused on SHLP2 and SHLP3 because they shared similar protective effects with HN. Specifically, they significantly reduced apoptosis and the generation of reactive oxygen species, and improved mitochondrial metabolism in vitro. SHLP2 and SHLP3 also enhanced 3T3-L1 pre-adipocyte differentiation. Systemic hyperinsulinemic-euglycemic clamp studies showed that intracerebrally infused SHLP2 increased glucose uptake and suppressed hepatic glucose production, suggesting that it functions as an insulin sensitizer both peripherally and centrally. Similar to HN, the levels of circulating SHLP2 were found to decrease with age. These results suggest that mitochondria play critical roles in metabolism and survival through the synthesis of mitochondrial peptides, and provide new insights into mitochondrial biology with relevance to aging and human biology.

Human mitochondrial DNA (mtDNA) is a double-stranded, circular molecule of 16,569 bp and contains 37 genes encoding 13 proteins, 22 tRNAs, and 2 rRNAs. Recent mitochondrial transcriptome analyses revealed the existence of small RNAs derived from mtDNA [1]. In 2001, Nishimoto and colleagues identified humanin (HN), a 24-amino-acid peptide encoded from the 16S ribosomal RNA (rRNA) region of mtDNA. HN is a potent neuroprotective factor capable of antagonizing Alzheimer’s disease (AD)-related cellular insults [2]. HN is a component of a novel retrograde signaling pathway from the mitochondria to the nucleus, which is distinct from mitochondrial signaling pathways, such as the SIRT4-AMPK pathway [3]. HN-dependent cellular protection is mediated in part by interacting with and antagonizing pro-apoptotic Bax-related peptides [4] and IGFBP-3 (IGF binding protein 3) [5].

Because of their involvement in energy production and free radical generation, mitochondria likely play a major role in aging and age-related diseases [68]. In fact, improvement of mitochondrial function has been shown to ameliorate age-related memory loss in aged mice [9]. Recent studies have shown that HN levels decrease with age, suggesting that HN could play a role in aging and age-related diseases, such as Alzheimer’s disease (AD), atherosclerosis, and diabetes. Along with lower HN levels in the hypothalamus, skeletal muscle, and cortex of older rodents, the circulating levels of HN were found to decline with age in both humans and mice [10]. Notably, circulating HN levels were found to be (i) significantly higher in long-lived Ames dwarf mice but lower in short-lived growth hormone (GH) transgenic mice, (ii) significantly higher in a GH-deficient cohort of patients with Laron syndrome, and (iii) reduced in mice and humans treated with GH or IGF-1 (insulin-like growth factor 1) [11]. Age-dependent declines in the circulating HN levels may be due to higher levels of reactive oxygen species (ROS) that contribute to atherosclerosis development. Using mouse models of atherosclerosis, it was found that HN-treated mice had a reduced disease burden and significant health improvements [12,13]. In addition, HN improved insulin sensitivity, suggesting clinical potential for mitochondrial peptides in diseases of aging [10]. The discovery of HN represents a unique addition to the spectrum of roles that mitochondria play in the cell [14,15]. A second mitochondrial-derived peptide (MDP), MOTS-c (mitochondrial open reading frame of the 12S rRNA-c), has also been shown to have metabolic effects on muscle and may also play a role in aging [16].

We further investigated mtDNA for the presence of other MDPs. Recent technological advances have led to the identification of small open reading frames (sORFs) in the nuclear genomes ofDrosophila[17,18] and mammals [19,20]. Therefore, we attempted to identify novel sORFs using the following approaches: 1) in silico identification of potential sORFs; 2) determination of mRNA expression levels; 3) development of specific antibodies against these novel peptides to allow for peptide detection in cells, organs, and plasma; 4) elucidating the actions of these peptides by performing cell-based assays for mitochondrial function, signaling, viability, and differentiation; and 5) delivering these peptides in vivo to determine their systemic metabolic effects. Focusing on the 16S rRNA region of the mtDNA where the humanin gene is located, we identified six sORFs and named them small humanin-like peptides (SHLPs) 1-6. While surveying the biological effects of SHLPs, we found that SHLP2 and SHLP3 were cytoprotective; therefore, we investigated their effects on apoptosis and metabolism in greater detail. Further, we showed that circulating SHLP2 levels declined with age, similar to HN, suggesting that SHLP2 is involved in aging and age-related disease progression.

SHLP2 and SHLP3 regulate the expression of metabolic and inflammatory markers

Epidemiological studies have demonstrated that increased levels of mediators of inflammation and acute-phase reactants, such as fibrinogen, C-reactive protein (CRP), and IL-6, correlate with the incidence of type 2 diabetes mellitus (T2DM) [3436]. In humans, anti-inflammatory drugs, such as aspirin and sodium salicylate, reduce fasting plasma glucose levels and ameliorate the symptoms of T2DM. In addition, anti-diabetic drugs, such as fibrates [37] and thiazolidinediones [38], have been found to lower some markers of inflammation. SHLP2 increased the levels of leptin, which is known to improve insulin sensitivity, but had no effect on the levels of the pro-inflammatory cytokines IL-6 and MCP-1. SHLP3 significantly increased the leptin levels, but also elevated IL-6 and MCP-1 levels, which could explain the lack of an in vivo insulin-sensitizing effect of SHLP3. The mechanism by which SHLPs regulate the expression of metabolic and inflammatory markers remains unclear and needs to be further investigated. Furthermore, SHLPs have different effects on inflammatory marker expression, suggesting differential regulation and function of individual SHLPs.

SHLP2 in aging

Mitochondria have been implicated in increased lifespan in several life-extending treatments [39,40]; however, it is not known whether the relationship is correlative or causative [40]. Additionally, it is well known that hormone levels change with aging. For example, levels of aldosterone, calcitonin, growth hormone, and IGF-I decrease with age. Circulating HN levels decline with age in humans and rodents, specifically in the hypothalamus and skeletal muscle of older rats. These changes parallel increases in the incidence of age-associated diseases such as AD and T2DM. The decline in circulating SHLP2 levels with age (Fig. 6), the anti-oxidative stress function of SHLP2 (Fig. 3C), and its neuroprotective effect (Fig. 6B) indicate that SHLP2 has a role in the regulation of aging and age-related diseases.

Conclusion

By analyzing the mitochondrial transcriptome, we found that sORFs from mitochondrial DNA encode functional peptides. We identified many mRNA transcripts within 13 protein-coding mitochondrial genes [1]. Such previously underappreciated sORFs have also been described in the nuclear genome [41]. The MDPs we describe here may represent retrograde communication signals from the mitochondria to the nucleus and may explain important aspects of mitochondrial biology that are implicated in health and longevity.

Larry, John Walker is working on mt proteins dynamics. His rotor – stator mechanism in ATPase synthase, a ‘complex’ that biologist accepted as energy generator is likely wrong. I was suppose to have met him in Germany few years ago. Energy in biological systems has nothing to do with heat. Heat is an outcome of a reaction, meaning that IR spectra accordingly to wave theory is a source of information memorized in water interference with carbon open systems within protein and glyo-proteins complexes as well as genome space-time outcomes. Physically speaking from a pure perspective of science ATP is highly unstable form of phosphate ‘chains’. It cannot hold energy, it is actually in contrary, it is like a resonator, trapping negativity, thus functioning as space propeller by expanding carbon skeleton of protein ‘machines’ Now, we don’t know what is ‘aging’ in a pure physical sense, except that we observe structural changes in what we call complexes. We we know is that proteins are not stationary structures, but highly dynamic forms of matter, seemingly occupying discrete and relative spaces. A piece of mt ATP ase could be discovered in the nucleus as transcription factor. Our notion of operational space in terms of electro dynamics from a motor – stator perspective is now translated toward defining semi conducting and supracoductive strings. The reality of which is so much more fascinating and beautiful as time progresses overally. There are spaces where time does not change, and there are spaces where time walks, and there are spaces, where time flies, and there are spaces where time runs. Amazing, indeed! The story of aging gets a lot deeper that science could even imagine, probably to roots of immortal energy- spaces. We know that matter is transient, that is nearly all living matter, replenishes of about 3 to 7 weeks.

Take a glass full of some kind of liquid, you know the mass of the glass and the mass of the liquid (say wine, beer, water, or milk) You also know to an approximate reality the composition of both. Now lift the glass full of liquid and let it break on a surface of your choice. Depending on the surface pieces of the glass would travel differential from a center projected by the vertical axis of your hand. What technology does today is recollecting those pieces and modelling them to fit in a form again that would resemble a holding device, a glass. The liquid we don’t know exactly how it spilled due the nature of its absorbancy of both surface physics and physical ‘state’ properties. Thus we can say how much approximate energy we have held thinking of m/z as time flight objectives. Each technology can read 1D and approximate the 2D, absolutely lacking computational methodology for 3D dynamic reality. Many scientists confuse space and volume. Volume is a one dimensional characteristic! So is crystalography! BY taking quantum chemical method computing principles following imaginative rules we could approach 2D, however , that is not enough to define 3D. Time we use as a reference frame of clocks we have invented in order to keep track of a sense to observable ‘change’ . But remember, time is absolute and parallel in continuity while energy is discrete , coming in quantum packages, realization of accumulated information. Information is highly redundant we see, so annotating information is an objective to modern days simulations that could predict outcomes of possible parallel realities we call worlds. One could ‘jump’ from one reality to another through guidance of light and water, but what remains unsolved is why people make mistakes, constantly by accusing in name of greed and power , or disobedience of commandments of the Lord!

On Thu, Apr 21, 2016 at 3:41 AM, Leaders in Pharmaceutical Business Intelligence (LPBI) Group wrote:

> larryhbern posted: “New Insights into mtDNA, mitochondrial proteins, > aging, and metabolic control Larry H. Bernstein, MD, FCAP, Curator LPBI > Newly discovered proteins may protect against age-related illnesses The > proteins could play a key role in the ” >

 

Metabolic features of the cell danger response
– Mitochondria in Health and Disease

Mitochondrion  Volume 16, May 2014, Pages 7–17     doi:10.1016/j.mito.2013.08.006

 

Highlights

  •  The Cell Danger Response (CDR) is defined in terms of an ancient metabolic response to threat.
  •  The CDR encompasses inflammation, innate immunity, oxidative stress, and the ER stress response.
  •  The CDR is maintained by extracellular nucleotide (purinergic) signaling.
  •  Abnormal persistence of the CDR lies at the heart of many chronic diseases.
  •  Antipurinergic therapy (APT) has proven effective in many chronic disorders in animal models

The cell danger response (CDR) is the evolutionarily conserved metabolic response that protects cells and hosts from harm. It is triggered by encounters with chemical, physical, or biological threats that exceed the cellular capacity for homeostasis. The resulting metabolic mismatch between available resources and functional capacity produces a cascade of changes in cellular electron flow, oxygen consumption, redox, membrane fluidity, lipid dynamics, bioenergetics, carbon and sulfur resource allocation, protein folding and aggregation, vitamin availability, metal homeostasis, indole, pterin, 1-carbon and polyamine metabolism, and polymer formation. The first wave of danger signals consists of the release of metabolic intermediates like ATP and ADP, Krebs cycle intermediates, oxygen, and reactive oxygen species (ROS), and is sustained by purinergic signaling. After the danger has been eliminated or neutralized, a choreographed sequence of anti-inflammatory and regenerative pathways is activated to reverse the CDR and to heal. When the CDR persists abnormally, whole body metabolism and the gut microbiome are disturbed, the collective performance of multiple organ systems is impaired, behavior is changed, and chronic disease results. Metabolic memory of past stress encounters is stored in the form of altered mitochondrial and cellular macromolecule content, resulting in an increase in functional reserve capacity through a process known as mitocellular hormesis. The systemic form of the CDR, and its magnified form, the purinergic life-threat response (PLTR), are under direct control by ancient pathways in the brain that are ultimately coordinated by centers in the brainstem. Chemosensory integration of whole body metabolism occurs in the brainstem and is a prerequisite for normal brain, motor, vestibular, sensory, social, and speech development. An understanding of the CDR permits us to reframe old concepts of pathogenesis for a broad array of chronic, developmental, autoimmune, and degenerative disorders. These disorders include autism spectrum disorders (ASD), attention deficit hyperactivity disorder (ADHD), asthma, atopy, gluten and many other food and chemical sensitivity syndromes, emphysema, Tourette’s syndrome, bipolar disorder, schizophrenia, post-traumatic stress disorder (PTSD), chronic traumatic encephalopathy (CTE), traumatic brain injury (TBI), epilepsy, suicidal ideation, organ transplant biology, diabetes, kidney, liver, and heart disease, cancer, Alzheimer and Parkinson disease, and autoimmune disorders like lupus, rheumatoid arthritis, multiple sclerosis, and primary sclerosing cholangitis.

The double face of mitochondrial dysfunction

Dmitry Knorre, Anna Zyrina, and Fedor Severin

pp 420-420

Full text | PDF

 

 

Flawed Mitochondrial DNA Could Undermine Stem Cell Therapies

http://www.genengnews.com/gen-news-highlights/flawed-mitochondrial-dna-could-undermine-stem-cell-therapies/81252622/

http://www.genengnews.com/Media/images/GENHighlight/thumb_Apr18_2016_OHSU_ConfocalMicroscopyImage7543773219.jpg

This is a confocal microscopy image of human fibroblasts derived from embryonic stem cells. The nuclei appear in blue, while smaller and more numerous mitochondria appear in red. [Shoukhrat Mitalipov]

Mutations in our mitochondrial DNA tend to be inconspicuous, but they can become more prevalent as we age. They can even vary in frequency from cell to cell. Naturally, some cells will be relatively compromised because they happen to have a higher percentage of mutated mitochondrial DNA. Such cells make a poor basis for stem cell lines. They should be excluded. But how?

To answer this question, a team of scientists scrutinized skin fibroblasts, blood cells, and induced pluripotent stem cells (iPSCs) for mitochondrial genome integrity. When the scientists tested the samples for mitochondrial DNA mutations, the levels of mutations appeared low. But when the scientists sequenced the iPS cell lines, they found higher numbers of mitochondrial DNA mutations, particularly in cells from patients over 60.

The scientists were led by Shoukhrat Mitalipov, Ph.D., director of the Center for Embryonic Cell and Gene Therapy at Oregon Health & Science University, and Taosheng Huang, M.D., a medical geneticist and director of the Mitochondrial Medicine Program at Cincinnati Children’s Hospital. The Mitalipov/Huang-led team also found higher percentages of mitochondria containing mutations within a cell. The higher the load of mutated mitochondrial DNA in a cell, the more compromised the cell’s function.

Since each iPSC line is created from a different cell, each line may contain different types of mitochondrial DNA mutations and mutation loads. To choose the least damaged line, the authors recommend screening multiple lines per patient. “It’s a good idea to check the iPS clones for mitochondrial DNA mutations and make sure you pick a good cell line,” said Dr. Huang.

This recommendation appeared April 14 in the journal Cell Stem Cell, in an article entitled, “Age-Related Accumulation of Somatic Mitochondrial DNA Mutations in Adult-Derived Human iPSCs.” This article holds that mitochondrial genome integrity is a vital readout in assessing the proficiency of patient-derived regenerative products destined for clinical applications.

“We found that pooled skin and blood mtDNA contained low heteroplasmic point mutations, but a panel of ten individual iPSC lines from each tissue or clonally expanded fibroblasts carried an elevated load of heteroplasmic or homoplasmic mutations, suggesting that somatic mutations randomly arise within individual cells but are not detectable in whole tissues,” wrote the article’s authors. “The frequency of mtDNA defects in iPSCs increased with age, and many mutations were nonsynonymous or resided in RNA coding genes and thus can lead to respiratory defects.”

Potential therapies using stem cells hold tremendous promise for treating human disease. However, defects in the mitochondria could undermine the iPS cells’ ability to repair damaged tissue or organs.

“If you want to use iPS cells in a human, you must check for mutations in the mitochondrial genome,” declared Dr. Huang. “Every single cell can be different. Two cells next to each other could have different mutations or different percentages of mutations.”

Prior to the creation of a therapeutic iPS cell line, a collection of cells is taken from the patient. These cells will be tested for mutations. If the tester uses Sanger sequencing, older technology that is not as sensitive as newer next-generation sequencing, any mutation that occurs in less than 20% of the sample will go undetected. But mitochondrial DNA mutations might occur in less than 20% of mitochondria in the pooled cells. As a result, mutation rates have not been well understood. “These mitochondrial mutations are actually hidden,” explained Dr. Mitalipov.

The mitochondrial genome is relatively small, containing just 37 genes, so screening should be feasible using next generation sequencing, Dr. Mitalipov added. “It should be relatively cheap and do-able.”

Dr. Mitalipov also commented on a more general point, the implications of the current study on illuminating the mechanisms of age-related disease: “Pathogenic mutations in our mitochondrial DNA have long been thought to be a driving force in aging and age-onset diseases, though clear evidence was missing. This foundational knowledge of how cells are damaged in the natural process of aging may help to illuminate the role of mutated mitochondria in degenerative disease.”

New Mitalipov paper on stem cell mitochondria: challenge for IPS cell field?

http://www.ipscell.com/tag/age-related-accumulation-of-somatic-mitochondrial-dna-mutations-in-adult-derived-human-ipscs/

A new paper from Shoukhrat Mitalipov’s lab on stem cell mitochondria points to a pattern whereby induced pluripotent stem (IPS) cells tend to have more problems if they are from older patients.

What does this paper mean for the stem cell field and could it impact more specifically the clinical applications of IPS cells?

http://i0.wp.com/www.ipscell.com/wp-content/uploads/2016/04/Mitalipov-mitochondrial-mutations.jpg?resize=300%2C295

Graphical Abstract, Kang, et al. 2016

The new paper Kang, et al is entitled “Age-Related Accumulation of Somatic Mitochondrial DNA Mutations in Adult-Derived Human iPSCs”.

This paper reminds us of the very important realities that mitochondria are key players in stem cell function and that mitochondria have their own genomes that impact that function. A lot of us don’t think about mitochondria and their genome as often as we should.

The paper came to three major scientific conclusions (this from the Highlights section of the paper and also see the graphical abstract for a visual sense of the results overall):

  • Human iPSC clones derived from elderly adults show accumulation of mtDNA mutations
  • Fewer mtDNA mutations are present in ESCs and iPSCs derived from younger adults
  • Accumulated mtDNA mutations can impact metabolic function in iPSCs

Importantly the team looked at IPS cells derived from both blood and skin cells and found that the former were less likely to have mitochondrial mutations.

This study suggests that those teams producing or working with human IPS cells (hIPSCs) should be screening the different lines for mitochondrial mutations. This excellent piece from Sara Reardon on the Mitalipov paper quotes IPS cell expert Jeanne Loring on this very point:

“It’s one of those things most of us don’t think about,” says Jeanne Loring, a stem-cell biologist at the Scripps Research Institute in La Jolla, California. Her lab is working towards using iPS cells to treat Parkinson’s disease, and Loring now plans to go back and examine the mitochondria in her cell lines. She suspects that it will be fairly easy for researchers to screen cells for use in therapies.”

Mitalipov goes further and suggests that his team’s new findings could support the use of human embryonic stem cells (hESC) derived by somatic cell nuclear transfer (SCNT) which would be expected to have mitochondria with fewer mutations. However, as Loring points out in the Reardon article, SCNT is really difficult to successfully perform and only a few labs in the world can do it at present. In that context, working with hIPSC and adding on the additional layer of mitochondrial DNA mutation screening could be more practical.

New York stem cell researcher Dieter Egli, however, is quoted that hIPSC have other differences with hESC as well such as epigenetic differences and he’s quoted in the Reardon piece, “It’s going to be very hard to find a cell line that’s perfect.”

One might reasonably ask both Egli and oneself, “What is a perfect cell line”?

In the end the best approach for use of human pluripotent stem cells of any kind is going to involve a balance between practicality of production and the potentially positive or negative traits of those cells as determined by rigorous validation screening.

With this new paper we’ve just learned more about another layer of screening that is needed. An interesting question is whether adult stem cells such as mesenchymal stromal/stem cells (MSC) also should be screened for mitochondrial mutations. They are often produced from patients who are getting up there in years. I hope that someone will publish on that too.

As to pluripotent cells, I expect that sometimes the best lines, meaning those most perfect for a given clinical application, will be hIPSC (autologous or allogeneic in some instances) and in other cases they may be hESC made from leftover IVF embryos. If SCNT-derived hESC can be more widely produced in an affordable manner and they pass validation as well then those (sometimes called NT-hESC) may also come into play clinically. So far that hasn’t happened for the SCNT cells, but it may over time.   …..

 Age-Related Accumulation of Somatic Mitochondrial DNA Mutations in Adult-Derived Human iPSCs

Eunju Kang, Xinjian Wang, Rebecca Tippner-Hedges, …, Don P. Wolf, Taosheng Huang, Shoukhrat Mitalipov
http://www.cell.com/cell-stem-cell/pdfExtended/S1934-5909(16)00067-9

In Brief Mitalipov, Huang, and colleagues show that human iPSCs derived from older adults carry more mitochondrial DNA mutations than those derived from younger individuals. Defects in metabolic function caused by mtDNA mutations suggest careful screening of hiPSC clones for mutational load before clinical application.

Highlights

  1. Human iPSC clones derived from elderly adults show accumulation of mtDNA mutations
  2. Fewer mtDNA mutations are present in ESCs and iPSCs derived from younger adults
  3. Accumulated mtDNA mutations can impact metabolic function in iPSCs

Kang et al., 2016, Cell Stem Cell 18, 1–12 May 5, 2016 ª2016 Elsevier Inc. http://dx.doi.org/10.1016/j.stem.2016.02.005

The genetic integrity of iPSCs is an important consideration for therapeutic application. In this study, we examine the accumulation of somatic mitochondrial genome (mtDNA) mutations in skin fibroblasts, blood, and iPSCs derived from young and elderly subjects (24–72 years). We found that pooled skin and blood mtDNA contained low heteroplasmic point mutations, but a panel of ten individual iPSC lines from each tissue or clonally expanded fibroblasts carried an elevated load of heteroplasmic or homoplasmic mutations, suggesting that somatic mutations randomly arise within individual cells but are not detectable in whole tissues. The frequency of mtDNA defects in iPSCs increased with age, and many mutations were non-synonymous or resided in RNA coding genes and thus can lead to respiratory defects. Our results highlight a need to monitor mtDNA mutations in iPSCs, especially those generated from older patients, and to examine the metabolic status of iPSCs destined for clinical applications.

Induced pluripotent stem cells (iPSCs) offer an unlimited source for autologous cell replacement therapies to treat age-associated degenerative diseases. Aging is generally characterized by increased DNA damage and genomic instability (Garinis et al., 2008; Lombard et al., 2005); thus, iPSCs derived from elderly subjects may harbor point mutations and larger genomic rearrangements. Indeed, iPSCs display increased chromosome aberrations (Mayshar et al., 2010), subchromosomal copy number variations (CNVs) (Abyzov et al., 2012; Laurent et al., 2011), and exome mutations (Johannesson et al., 2014), compared to natural embryonic stem cell (ESC) counterparts (Ma et al., 2014). The rate of mtDNA mutations is believed to be at least 10- to 20-fold higher than that observed in the nuclear genome (Wallace, 1994), and often both mutated and wild-type mtDNA (heteroplasmy) can coexist in the same cell (Rossignol et al., 2003). Large deletions are most frequently observed mtDNA abnormalities in aged post-mitotic tissues such as brain, heart, and muscle (Bender et al., 2006; Bua et al., 2006; Corral-Debrinski et al., 1992; Cortopassi et al., 1992; Mohamed et al., 2006) and have been implicated in aging and diseases such as Alzheimer’s disease (AD), Parkinson’s disease (PD), amyotrophic lateral sclerosis (ALS), and diabetes (Larsson, 2010; Lin and Beal, 2006; Petersen et al., 2003; Wallace, 2005). In addition, mtDNA point mutations were reported in some tumors and replicating tissues (Chatterjee et al., 2006; Ju et al., 2014; Michikawa et al., 1999; Taylor et al., 2003). However, the extent of mtDNA defects in proliferating peripheral tissues commonly used for iPSC induction, such as skin and blood, is thought to be low and limited to common non-coding variants (Schon et al., 2012; Yao et al., 2015). Accumulation of mtDNA variants in these tissues with age was insignificant (Greaves et al., 2010; Hashizume et al., 2015). Several point mutations were identified in iPSCs generated from the newborn foreskin fibroblasts, although most of these variants were non-coding, common for the general population, and did not affect their metabolic activity (Prigione et al., 2011). Somatic mtDNA mutations may be under-reported secondary to the level of sample interrogation. …..

Figure 2. mtDNA Mutations in Skin Fibroblasts, Blood, and the iPSCs of a 72-YearOld B Subject (A) Sixteen mutations at low heteroplasmy levels were detected in the DNA of PF, while a panel of ten FiPSC lines carried nine mutations, including four that were homoplasmic. Gray rectangles define the mutations shared between PF and FiPSCs. (B) Venn diagram showing only one mutation in FiPSCs shared with PF. (C) All ten FiPSC lines carried between one and five high-heteroplasmy (>15%) mutations. (D) Mutation distribution in whole blood and BiPSCs was similar to that in PF and FiPSCs. Six mutations at low-heteroplasmy levels were observed in blood, while BiPSC lines displayed 21 mutations, including four over the 80% heteroplasmy level. (E) Venn diagram showing four mutations in BiPSCs shared with whole blood and the 17 novel variants. (F) Distribution of mutations in individual BiPSC lines. See also Figures S2 and S3; Table S1; Table S3, sheet 2; and Table S4, sheet 1   ….

Figure 4. Transmission and Distribution of Somatic mtDNA Mutations to iPSCs (A) A total of 112 mtDNA mutations were discovered in parental cells (PF, CF, and blood) from 11 subjects. Of these, 39 variants (35%) were found in corresponding 130 iPSC lines. Among non-transmitted, transmitted, and novel mutations in iPSCs, comparable percentages of variants (68%, 69%, and 79%, respectively) were coding mutations in protein, rRNA, or tRNA genes. This suggests that most pathogenic mutations do not affect iPSC induction. However, certain coding mutations including in ND3, ND4L, and 14 tRNA genes were not detected in iPSCs, suggesting possible pathogenicity. n, the number of mtDNA mutations. Blue font genes were detected in parental cells. (B–D) A total of 80 high heteroplasmic (>15%) variants were detected in the present study in 130 FiPSC or BiPSC lines from 11 subjects. (B) The majority of these variants (76%) were non-synonymous or frame-shift mutations in protein-coding genes or affected rRNA and tRNA genes. (C) More than half of the mutations (56%) were never reported in a database containing whole mtDNA sequences from 26,850 healthy subjects representing the general human population (http://www.mitomap.org/MITOMAP). (D) Most mutations (90%) were never reported in a database containing sequences from healthy subjects with corresponding mtDNA haplotypes. freq., frequent. See also Figure S5 and Tables S3 and S4. ….

sjwilliamspa

Mutations will accumulate over age in mitochondrial DNA, however the current study has the difficulty that the authors could not use patient-age-matched controls, in essence they could only compare induced pluripotent stem cells derived from different patients. This could confound the results but the result with higher frequency of mutation in mtDNA in cells reprogrammed from younger patients is interesting but might limit the ability of autologous regenerative therapy in older patients. However reprogramming, although the method not mentioned here although I am assuming by transfection with lentivirus is a rough procedure, involving multiple dedifferentiation steps. Therefore it is very understandable that cells obtained from elderly patients would respond less favorably to such a rough reprogramming regimen, especially if it produced a higher degree of ROS, which has been shown to alter mtDNA. This is why I feel it is more advantageous to obtain a stem cell population from fat cells and forgo the Oct4, htert, reprogramming with lentiviral vectors.

 

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Imaging of Cancer Cells, Volume 2 (Volume Two: Latest in Genomics Methodologies for Therapeutics: Gene Editing, NGS and BioInformatics, Simulations and the Genome Ontology), Part 1: Next Generation Sequencing (NGS)

Imaging of Cancer Cells

Larry H. Bernstein, MD, FCAP, Curator

LPBI

 

Microscope uses nanosecond-speed laser and deep learning to detect cancer cells more efficiently

April 13, 2016

Scientists at the California NanoSystems Institute at UCLA have developed a new technique for identifying cancer cells in blood samples faster and more accurately than the current standard methods.

In one common approach to testing for cancer, doctors add biochemicals to blood samples. Those biochemicals attach biological “labels” to the cancer cells, and those labels enable instruments to detect and identify them. However, the biochemicals can damage the cells and render the samples unusable for future analyses. There are other current techniques that don’t use labeling but can be inaccurate because they identify cancer cells based only on one physical characteristic.

Time-stretch quantitative phase imaging (TS-QPI) and analytics system

The new technique images cells without destroying them and can identify 16 physical characteristics — including size, granularity and biomass — instead of just one.

The new technique combines two components that were invented at UCLA:

A “photonic time stretch” microscope, which is capable of quickly imaging cells in blood samples. Invented by Barham Jalali, professor and Northrop-Grumman Optoelectronics Chair in electrical engineering, it works by taking pictures of flowing blood cells using laser bursts (similar to how a camera uses a flash). Each flash only lasts nanoseconds (billionths of a second) to avoid damage to cells, but that normally means the images are both too weak to be detected and too fast to be digitized by normal instrumentation. The new microscope overcomes those challenges by using specially designed optics that amplify and boost the clarity of the images, and simultaneously slow them down enough to be detected and digitized at a rate of 36 million images per second.

A deep learning computer program, which identifies cancer cells with more than 95 percent accuracy. Deep learning is a form of artificial intelligence that uses complex algorithms to extract patterns and knowledge from rich multidimenstional datasets, with the goal of achieving accurate decision making.

The study was published in the open-access journal Nature Scientific Reports. The researchers write in the paper that the system could lead to data-driven diagnoses by cells’ physical characteristics, which could allow quicker and earlier diagnoses of cancer, for example, and better understanding of the tumor-specific gene expression in cells, which could facilitate new treatments for disease.

The research was supported by NantWorks, LLC.

 

Abstract of Deep Learning in Label-free Cell Classification

Label-free cell analysis is essential to personalized genomics, cancer diagnostics, and drug development as it avoids adverse effects of staining reagents on cellular viability and cell signaling. However, currently available label-free cell assays mostly rely only on a single feature and lack sufficient differentiation. Also, the sample size analyzed by these assays is limited due to their low throughput. Here, we integrate feature extraction and deep learning with high-throughput quantitative imaging enabled by photonic time stretch, achieving record high accuracy in label-free cell classification. Our system captures quantitative optical phase and intensity images and extracts multiple biophysical features of individual cells. These biophysical measurements form a hyperdimensional feature space in which supervised learning is performed for cell classification. We compare various learning algorithms including artificial neural network, support vector machine, logistic regression, and a novel deep learning pipeline, which adopts global optimization of receiver operating characteristics. As a validation of the enhanced sensitivity and specificity of our system, we show classification of white blood T-cells against colon cancer cells, as well as lipid accumulating algal strains for biofuel production. This system opens up a new path to data-driven phenotypic diagnosis and better understanding of the heterogeneous gene expressions in cells.

references:

Claire Lifan Chen, Ata Mahjoubfar, Li-Chia Tai, Ian K. Blaby, Allen Huang, Kayvan Reza Niazi & Bahram Jalali. Deep Learning in Label-free Cell Classification. Scientific Reports 6, Article number: 21471 (2016); doi:10.1038/srep21471 (open access)

Supplementary Information

 

Deep Learning in Label-free Cell Classification

Claire Lifan Chen, Ata Mahjoubfar, Li-Chia Tai, Ian K. Blaby, Allen Huang,Kayvan Reza Niazi & Bahram Jalali

Scientific Reports 6, Article number: 21471 (2016)    http://dx.doi.org:/10.1038/srep21471

Deep learning extracts patterns and knowledge from rich multidimenstional datasets. While it is extensively used for image recognition and speech processing, its application to label-free classification of cells has not been exploited. Flow cytometry is a powerful tool for large-scale cell analysis due to its ability to measure anisotropic elastic light scattering of millions of individual cells as well as emission of fluorescent labels conjugated to cells1,2. However, each cell is represented with single values per detection channels (forward scatter, side scatter, and emission bands) and often requires labeling with specific biomarkers for acceptable classification accuracy1,3. Imaging flow cytometry4,5 on the other hand captures images of cells, revealing significantly more information about the cells. For example, it can distinguish clusters and debris that would otherwise result in false positive identification in a conventional flow cytometer based on light scattering6.

In addition to classification accuracy, the throughput is another critical specification of a flow cytometer. Indeed high throughput, typically 100,000 cells per second, is needed to screen a large enough cell population to find rare abnormal cells that are indicative of early stage diseases. However there is a fundamental trade-off between throughput and accuracy in any measurement system7,8. For example, imaging flow cytometers face a throughput limit imposed by the speed of the CCD or the CMOS cameras, a number that is approximately 2000 cells/s for present systems9. Higher flow rates lead to blurred cell images due to the finite camera shutter speed. Many applications of flow analyzers such as cancer diagnostics, drug discovery, biofuel development, and emulsion characterization require classification of large sample sizes with a high-degree of statistical accuracy10. This has fueled research into alternative optical diagnostic techniques for characterization of cells and particles in flow.

Recently, our group has developed a label-free imaging flow-cytometry technique based on coherent optical implementation of the photonic time stretch concept11. This instrument overcomes the trade-off between sensitivity and speed by using Amplified Time-stretch Dispersive Fourier Transform12,13,14,15. In time stretched imaging16, the object’s spatial information is encoded in the spectrum of laser pulses within a pulse duration of sub-nanoseconds (Fig. 1). Each pulse representing one frame of the camera is then stretched in time so that it can be digitized in real-time by an electronic analog-to-digital converter (ADC). The ultra-fast pulse illumination freezes the motion of high-speed cells or particles in flow to achieve blur-free imaging. Detection sensitivity is challenged by the low number of photons collected during the ultra-short shutter time (optical pulse width) and the drop in the peak optical power resulting from the time stretch. These issues are solved in time stretch imaging by implementing a low noise-figure Raman amplifier within the dispersive device that performs time stretching8,11,16. Moreover, warped stretch transform17,18can be used in time stretch imaging to achieve optical image compression and nonuniform spatial resolution over the field-of-view19. In the coherent version of the instrument, the time stretch imaging is combined with spectral interferometry to measure quantitative phase and intensity images in real-time and at high throughput20. Integrated with a microfluidic channel, coherent time stretch imaging system in this work measures both quantitative optical phase shift and loss of individual cells as a high-speed imaging flow cytometer, capturing 36 million images per second in flow rates as high as 10 meters per second, reaching up to 100,000 cells per second throughput.

Figure 1: Time stretch quantitative phase imaging (TS-QPI) and analytics system; A mode-locked laser followed by a nonlinear fiber, an erbium doped fiber amplifier (EDFA), and a wavelength-division multiplexing (WDM) filter generate and shape a train of broadband optical pulses. http://www.nature.com/article-assets/npg/srep/2016/160315/srep21471/images_hires/m685/srep21471-f1.jpg

 

Box 1: The pulse train is spatially dispersed into a train of rainbow flashes illuminating the target as line scans. The spatial features of the target are encoded into the spectrum of the broadband optical pulses, each representing a one-dimensional frame. The ultra-short optical pulse illumination freezes the motion of cells during high speed flow to achieve blur-free imaging with a throughput of 100,000 cells/s. The phase shift and intensity loss at each location within the field of view are embedded into the spectral interference patterns using a Michelson interferometer. Box 2: The interferogram pulses were then stretched in time so that spatial information could be mapped into time through time-stretch dispersive Fourier transform (TS-DFT), and then captured by a single pixel photodetector and an analog-to-digital converter (ADC). The loss of sensitivity at high shutter speed is compensated by stimulated Raman amplification during time stretch. Box 3: (a) Pulse synchronization; the time-domain signal carrying serially captured rainbow pulses is transformed into a series of one-dimensional spatial maps, which are used for forming line images. (b) The biomass density of a cell leads to a spatially varying optical phase shift. When a rainbow flash passes through the cells, the changes in refractive index at different locations will cause phase walk-off at interrogation wavelengths. Hilbert transformation and phase unwrapping are used to extract the spatial phase shift. (c) Decoding the phase shift in each pulse at each wavelength and remapping it into a pixel reveals the protein concentration distribution within cells. The optical loss induced by the cells, embedded in the pulse intensity variations, is obtained from the amplitude of the slowly varying envelope of the spectral interferograms. Thus, quantitative optical phase shift and intensity loss images are captured simultaneously. Both images are calibrated based on the regions where the cells are absent. Cell features describing morphology, granularity, biomass, etc are extracted from the images. (d) These biophysical features are used in a machine learning algorithm for high-accuracy label-free classification of the cells.

On another note, surface markers used to label cells, such as EpCAM21, are unavailable in some applications; for example, melanoma or pancreatic circulating tumor cells (CTCs) as well as some cancer stem cells are EpCAM-negative and will escape EpCAM-based detection platforms22. Furthermore, large-population cell sorting opens the doors to downstream operations, where the negative impacts of labels on cellular behavior and viability are often unacceptable23. Cell labels may cause activating/inhibitory signal transduction, altering the behavior of the desired cellular subtypes, potentially leading to errors in downstream analysis, such as DNA sequencing and subpopulation regrowth. In this way, quantitative phase imaging (QPI) methods24,25,26,27 that categorize unlabeled living cells with high accuracy are needed. Coherent time stretch imaging is a method that enables quantitative phase imaging at ultrahigh throughput for non-invasive label-free screening of large number of cells.

In this work, the information of quantitative optical loss and phase images are fused into expert designed features, leading to a record label-free classification accuracy when combined with deep learning. Image mining techniques are applied, for the first time, to time stretch quantitative phase imaging to measure biophysical attributes including protein concentration, optical loss, and morphological features of single cells at an ultrahigh flow rate and in a label-free fashion. These attributes differ widely28,29,30,31 among cells and their variations reflect important information of genotypes and physiological stimuli32. The multiplexed biophysical features thus lead to information-rich hyper-dimensional representation of the cells for label-free classification with high statistical precision.

We further improved the accuracy, repeatability, and the balance between sensitivity and specificity of our label-free cell classification by a novel machine learning pipeline, which harnesses the advantages of multivariate supervised learning, as well as unique training by evolutionary global optimization of receiver operating characteristics (ROC). To demonstrate sensitivity, specificity, and accuracy of multi-feature label-free flow cytometry using our technique, we classified (1) OT-IIhybridoma T-lymphocytes and SW-480 colon cancer epithelial cells, and (2) Chlamydomonas reinhardtii algal cells (herein referred to as Chlamydomonas) based on their lipid content, which is related to the yield in biofuel production. Our preliminary results show that compared to classification by individual biophysical parameters, our label-free hyperdimensional technique improves the detection accuracy from 77.8% to 95.5%, or in other words, reduces the classification inaccuracy by about five times.     ……..

 

Feature Extraction

The decomposed components of sequential line scans form pairs of spatial maps, namely, optical phase and loss images as shown in Fig. 2 (see Section Methods: Image Reconstruction). These images are used to obtain biophysical fingerprints of the cells8,36. With domain expertise, raw images are fused and transformed into a suitable set of biophysical features, listed in Table 1, which the deep learning model further converts into learned features for improved classification.

The new technique combines two components that were invented at UCLA:

A “photonic time stretch” microscope, which is capable of quickly imaging cells in blood samples. Invented by Barham Jalali, professor and Northrop-Grumman Optoelectronics Chair in electrical engineering, it works by taking pictures of flowing blood cells using laser bursts (similar to how a camera uses a flash). Each flash only lasts nanoseconds (billionths of a second) to avoid damage to cells, but that normally means the images are both too weak to be detected and too fast to be digitized by normal instrumentation. The new microscope overcomes those challenges by using specially designed optics that amplify and boost the clarity of the images, and simultaneously slow them down enough to be detected and digitized at a rate of 36 million images per second.

A deep learning computer program, which identifies cancer cells with more than 95 percent accuracy. Deep learning is a form of artificial intelligence that uses complex algorithms to extract patterns and knowledge from rich multidimenstional datasets, with the goal of achieving accurate decision making.

The study was published in the open-access journal Nature Scientific Reports. The researchers write in the paper that the system could lead to data-driven diagnoses by cells’ physical characteristics, which could allow quicker and earlier diagnoses of cancer, for example, and better understanding of the tumor-specific gene expression in cells, which could facilitate new treatments for disease.

The research was supported by NantWorks, LLC.

 

http://www.nature.com/article-assets/npg/srep/2016/160315/srep21471/images_hires/m685/srep21471-f2.jpg

The optical loss images of the cells are affected by the attenuation of multiplexed wavelength components passing through the cells. The attenuation itself is governed by the absorption of the light in cells as well as the scattering from the surface of the cells and from the internal cell organelles. The optical loss image is derived from the low frequency component of the pulse interferograms. The optical phase image is extracted from the analytic form of the high frequency component of the pulse interferograms using Hilbert Transformation, followed by a phase unwrapping algorithm. Details of these derivations can be found in Section Methods. Also, supplementary Videos 1 and 2 show measurements of cell-induced optical path length difference by TS-QPI at four different points along the rainbow for OT-II and SW-480, respectively.

Table 1: List of extracted features.

Feature Name    Description         Category

 

Figure 3: Biophysical features formed by image fusion.

(a) Pairwise correlation matrix visualized as a heat map. The map depicts the correlation between all major 16 features extracted from the quantitative images. Diagonal elements of the matrix represent correlation of each parameter with itself, i.e. the autocorrelation. The subsets in box 1, box 2, and box 3 show high correlation because they are mainly related to morphological, optical phase, and optical loss feature categories, respectively. (b) Ranking of biophysical features based on their AUCs in single-feature classification. Blue bars show performance of the morphological parameters, which includes diameter along the interrogation rainbow, diameter along the flow direction, tight cell area, loose cell area, perimeter, circularity, major axis length, orientation, and median radius. As expected, morphology contains most information, but other biophysical features can contribute to improved performance of label-free cell classification. Orange bars show optical phase shift features i.e. optical path length differences and refractive index difference. Green bars show optical loss features representing scattering and absorption by the cell. The best performed feature in these three categories are marked in red.

Figure 4: Machine learning pipeline. Information of quantitative optical phase and loss images are fused to extract multivariate biophysical features of each cell, which are fed into a fully-connected neural network.

The neural network maps input features by a chain of weighted sum and nonlinear activation functions into learned feature space, convenient for classification. This deep neural network is globally trained via area under the curve (AUC) of the receiver operating characteristics (ROC). Each ROC curve corresponds to a set of weights for connections to an output node, generated by scanning the weight of the bias node. The training process maximizes AUC, pushing the ROC curve toward the upper left corner, which means improved sensitivity and specificity in classification.

….   How to cite this article: Chen, C. L. et al. Deep Learning in Label-free Cell Classification.

Sci. Rep. 6, 21471; http://dx.doi.org:/10.1038/srep21471

 

Computer Algorithm Helps Characterize Cancerous Genomic Variations

http://www.genengnews.com/gen-news-highlights/computer-algorithm-helps-characterize-cancerous-genomic-variations/81252626/

To better characterize the functional context of genomic variations in cancer, researchers developed a new computer algorithm called REVEALER. [UC San Diego Health]

Scientists at the University of California San Diego School of Medicine and the Broad Institute say they have developed a new computer algorithm—REVEALER—to better characterize the functional context of genomic variations in cancer. The tool, described in a paper (“Characterizing Genomic Alterations in Cancer by Complementary Functional Associations”) published in Nature Biotechnology, is designed to help researchers identify groups of genetic variations that together associate with a particular way cancer cells get activated, or how they respond to certain treatments.

REVEALER is available for free to the global scientific community via the bioinformatics software portal GenePattern.org.

“This computational analysis method effectively uncovers the functional context of genomic alterations, such as gene mutations, amplifications, or deletions, that drive tumor formation,” said senior author Pablo Tamayo, Ph.D., professor and co-director of the UC San Diego Moores Cancer Center Genomics and Computational Biology Shared Resource.

Dr. Tamayo and team tested REVEALER using The Cancer Genome Atlas (TCGA), the NIH’s database of genomic information from more than 500 human tumors representing many cancer types. REVEALER revealed gene alterations associated with the activation of several cellular processes known to play a role in tumor development and response to certain drugs. Some of these gene mutations were already known, but others were new.

For example, the researchers discovered new activating genomic abnormalities for beta-catenin, a cancer-promoting protein, and for the oxidative stress response that some cancers hijack to increase their viability.

REVEALER requires as input high-quality genomic data and a significant number of cancer samples, which can be a challenge, according to Dr. Tamayo. But REVEALER is more sensitive at detecting similarities between different types of genomic features and less dependent on simplifying statistical assumptions, compared to other methods, he adds.

“This study demonstrates the potential of combining functional profiling of cells with the characterizations of cancer genomes via next-generation sequencing,” said co-senior author Jill P. Mesirov, Ph.D., professor and associate vice chancellor for computational health sciences at UC San Diego School of Medicine.

 

Characterizing genomic alterations in cancer by complementary functional associations

Jong Wook Kim, Olga B Botvinnik, Omar Abudayyeh, Chet Birger, et al.

Nature Biotechnology (2016)              http://dx.doi.org:/10.1038/nbt.3527

Systematic efforts to sequence the cancer genome have identified large numbers of mutations and copy number alterations in human cancers. However, elucidating the functional consequences of these variants, and their interactions to drive or maintain oncogenic states, remains a challenge in cancer research. We developed REVEALER, a computational method that identifies combinations of mutually exclusive genomic alterations correlated with functional phenotypes, such as the activation or gene dependency of oncogenic pathways or sensitivity to a drug treatment. We used REVEALER to uncover complementary genomic alterations associated with the transcriptional activation of β-catenin and NRF2, MEK-inhibitor sensitivity, and KRAS dependency. REVEALER successfully identified both known and new associations, demonstrating the power of combining functional profiles with extensive characterization of genomic alterations in cancer genomes

 

Figure 2: REVEALER results for transcriptional activation of β-catenin in cancer.close

(a) This heatmap illustrates the use of the REVEALER approach to find complementary genomic alterations that match the transcriptional activation of β-catenin in cancer. The target profile is a TCF4 reporter that provides an estimate of…

 

An imaging-based platform for high-content, quantitative evaluation of therapeutic response in 3D tumour models

Jonathan P. Celli, Imran Rizvi, Adam R. Blanden, Iqbal Massodi, Michael D. Glidden, Brian W. Pogue & Tayyaba Hasan

Scientific Reports 4; 3751  (2014)    http://dx.doi.org:/10.1038/srep03751

While it is increasingly recognized that three-dimensional (3D) cell culture models recapitulate drug responses of human cancers with more fidelity than monolayer cultures, a lack of quantitative analysis methods limit their implementation for reliable and routine assessment of emerging therapies. Here, we introduce an approach based on computational analysis of fluorescence image data to provide high-content readouts of dose-dependent cytotoxicity, growth inhibition, treatment-induced architectural changes and size-dependent response in 3D tumour models. We demonstrate this approach in adherent 3D ovarian and pancreatic multiwell extracellular matrix tumour overlays subjected to a panel of clinically relevant cytotoxic modalities and appropriately designed controls for reliable quantification of fluorescence signal. This streamlined methodology reads out the high density of information embedded in 3D culture systems, while maintaining a level of speed and efficiency traditionally achieved with global colorimetric reporters in order to facilitate broader implementation of 3D tumour models in therapeutic screening.

The attrition rates for preclinical development of oncology therapeutics are particularly dismal due to a complex set of factors which includes 1) the failure of pre-clinical models to recapitulate determinants of in vivo treatment response, and 2) the limited ability of available assays to extract treatment-specific data integral to the complexities of therapeutic responses1,2,3. Three-dimensional (3D) tumour models have been shown to restore crucial stromal interactions which are missing in the more commonly used 2D cell culture and that influence tumour organization and architecture4,5,6,7,8, as well as therapeutic response9,10, multicellular resistance (MCR)11,12, drug penetration13,14, hypoxia15,16, and anti-apoptotic signaling17. However, such sophisticated models can only have an impact on therapeutic guidance if they are accompanied by robust quantitative assays, not only for cell viability but also for providing mechanistic insights related to the outcomes. While numerous assays for drug discovery exist18, they are generally not developed for use in 3D systems and are often inherently unsuitable. For example, colorimetric conversion products have been noted to bind to extracellular matrix (ECM)19 and traditional colorimetric cytotoxicity assays reduce treatment response to a single number reflecting a biochemical event that has been equated to cell viability (e.g. tetrazolium salt conversion20). Such approaches fail to provide insight into the spatial patterns of response within colonies, morphological or structural effects of drug response, or how overall culture viability may be obscuring the status of sub-populations that are resistant or partially responsive. Hence, the full benefit of implementing 3D tumour models in therapeutic development has yet to be realized for lack of analytical methods that describe the very aspects of treatment outcome that these systems restore.

Motivated by these factors, we introduce a new platform for quantitative in situ treatment assessment (qVISTA) in 3D tumour models based on computational analysis of information-dense biological image datasets (bioimage-informatics)21,22. This methodology provides software end-users with multiple levels of complexity in output content, from rapidly-interpreted dose response relationships to higher content quantitative insights into treatment-dependent architectural changes, spatial patterns of cytotoxicity within fields of multicellular structures, and statistical analysis of nodule-by-nodule size-dependent viability. The approach introduced here is cognizant of tradeoffs between optical resolution, data sampling (statistics), depth of field, and widespread usability (instrumentation requirement). Specifically, it is optimized for interpretation of fluorescent signals for disease-specific 3D tumour micronodules that are sufficiently small that thousands can be imaged simultaneously with little or no optical bias from widefield integration of signal along the optical axis of each object. At the core of our methodology is the premise that the copious numerical readouts gleaned from segmentation and interpretation of fluorescence signals in these image datasets can be converted into usable information to classify treatment effects comprehensively, without sacrificing the throughput of traditional screening approaches. It is hoped that this comprehensive treatment-assessment methodology will have significant impact in facilitating more sophisticated implementation of 3D cell culture models in preclinical screening by providing a level of content and biological relevance impossible with existing assays in monolayer cell culture in order to focus therapeutic targets and strategies before costly and tedious testing in animal models.

Using two different cell lines and as depicted in Figure 1, we adopt an ECM overlay method pioneered originally for 3D breast cancer models23, and developed in previous studies by us to model micrometastatic ovarian cancer19,24. This system leads to the formation of adherent multicellular 3D acini in approximately the same focal plane atop a laminin-rich ECM bed, implemented here in glass-bottom multiwell imaging plates for automated microscopy. The 3D nodules resultant from restoration of ECM signaling5,8, are heterogeneous in size24, in contrast to other 3D spheroid methods, such as rotary or hanging drop cultures10, in which cells are driven to aggregate into uniformly sized spheroids due to lack of an appropriate substrate to adhere to. Although the latter processes are also biologically relevant, it is the adherent tumour populations characteristic of advanced metastatic disease that are more likely to be managed with medical oncology, which are the focus of therapeutic evaluation herein. The heterogeneity in 3D structures formed via ECM overlay is validated here by endoscopic imaging ofin vivo tumours in orthotopic xenografts derived from the same cells (OVCAR-5).

 

Figure 1: A simplified schematic flow chart of imaging-based quantitative in situ treatment assessment (qVISTA) in 3D cell culture.

(This figure was prepared in Adobe Illustrator® software by MD Glidden, JP Celli and I Rizvi). A detailed breakdown of the image processing (Step 4) is provided in Supplemental Figure 1.

A critical component of the imaging-based strategy introduced here is the rational tradeoff of image-acquisition parameters for field of view, depth of field and optical resolution, and the development of image processing routines for appropriate removal of background, scaling of fluorescence signals from more than one channel and reliable segmentation of nodules. In order to obtain depth-resolved 3D structures for each nodule at sub-micron lateral resolution using a laser-scanning confocal system, it would require ~ 40 hours (at approximately 100 fields for each well with a 20× objective, times 1 minute/field for a coarse z-stack, times 24 wells) to image a single plate with the same coverage achieved in this study. Even if the resources were available to devote to such time-intensive image acquisition, not to mention the processing, the optical properties of the fluorophores would change during the required time frame for image acquisition, even with environmental controls to maintain culture viability during such extended imaging. The approach developed here, with a mind toward adaptation into high throughput screening, provides a rational balance of speed, requiring less than 30 minutes/plate, and statistical rigour, providing images of thousands of nodules in this time, as required for the high-content analysis developed in this study. These parameters can be further optimized for specific scenarios. For example, we obtain the same number of images in a 96 well plate as for a 24 well plate by acquiring only a single field from each well, rather than 4 stitched fields. This quadruples the number conditions assayed in a single run, at the expense of the number of nodules per condition, and therefore the ability to obtain statistical data sets for size-dependent response, Dfrac and other segmentation-dependent numerical readouts.

 

We envision that the system for high-content interrogation of therapeutic response in 3D cell culture could have widespread impact in multiple arenas from basic research to large scale drug development campaigns. As such, the treatment assessment methodology presented here does not require extraordinary optical instrumentation or computational resources, making it widely accessible to any research laboratory with an inverted fluorescence microscope and modestly equipped personal computer. And although we have focused here on cancer models, the methodology is broadly applicable to quantitative evaluation of other tissue models in regenerative medicine and tissue engineering. While this analysis toolbox could have impact in facilitating the implementation of in vitro 3D models in preclinical treatment evaluation in smaller academic laboratories, it could also be adopted as part of the screening pipeline in large pharma settings. With the implementation of appropriate temperature controls to handle basement membranes in current robotic liquid handling systems, our analyses could be used in ultra high-throughput screening. In addition to removing non-efficacious potential candidate drugs earlier in the pipeline, this approach could also yield the additional economic advantage of minimizing the use of costly time-intensive animal models through better estimates of dose range, sequence and schedule for combination regimens.

 

Microscope Uses AI to Find Cancer Cells More Efficiently

Thu, 04/14/2016 – by Shaun Mason

http://www.mdtmag.com/news/2016/04/microscope-uses-ai-find-cancer-cells-more-efficiently

Scientists at the California NanoSystems Institute at UCLA have developed a new technique for identifying cancer cells in blood samples faster and more accurately than the current standard methods.

In one common approach to testing for cancer, doctors add biochemicals to blood samples. Those biochemicals attach biological “labels” to the cancer cells, and those labels enable instruments to detect and identify them. However, the biochemicals can damage the cells and render the samples unusable for future analyses.

There are other current techniques that don’t use labeling but can be inaccurate because they identify cancer cells based only on one physical characteristic.

The new technique images cells without destroying them and can identify 16 physical characteristics — including size, granularity and biomass — instead of just one. It combines two components that were invented at UCLA: a photonic time stretch microscope, which is capable of quickly imaging cells in blood samples, and a deep learning computer program that identifies cancer cells with over 95 percent accuracy.

Deep learning is a form of artificial intelligence that uses complex algorithms to extract meaning from data with the goal of achieving accurate decision making.

The study, which was published in the journal Nature Scientific Reports, was led by Barham Jalali, professor and Northrop-Grumman Optoelectronics Chair in electrical engineering; Claire Lifan Chen, a UCLA doctoral student; and Ata Mahjoubfar, a UCLA postdoctoral fellow.

Photonic time stretch was invented by Jalali, and he holds a patent for the technology. The new microscope is just one of many possible applications; it works by taking pictures of flowing blood cells using laser bursts in the way that a camera uses a flash. This process happens so quickly — in nanoseconds, or billionths of a second — that the images would be too weak to be detected and too fast to be digitized by normal instrumentation.

The new microscope overcomes those challenges using specially designed optics that boost the clarity of the images and simultaneously slow them enough to be detected and digitized at a rate of 36 million images per second. It then uses deep learning to distinguish cancer cells from healthy white blood cells.

“Each frame is slowed down in time and optically amplified so it can be digitized,” Mahjoubfar said. “This lets us perform fast cell imaging that the artificial intelligence component can distinguish.”

Normally, taking pictures in such minuscule periods of time would require intense illumination, which could destroy live cells. The UCLA approach also eliminates that problem.

“The photonic time stretch technique allows us to identify rogue cells in a short time with low-level illumination,” Chen said.

The researchers write in the paper that the system could lead to data-driven diagnoses by cells’ physical characteristics, which could allow quicker and earlier diagnoses of cancer, for example, and better understanding of the tumor-specific gene expression in cells, which could facilitate new treatments for disease.   …..  see also http://www.nature.com/article-assets/npg/srep/2016/160315/srep21471/images_hires/m685/srep21471-f1.jpg

Chen, C. L. et al. Deep Learning in Label-free Cell Classification.    Sci. Rep. 6, 21471;   http://dx.doi.org:/10.1038/srep21471

 

 

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Prions and protein misfolding disorders

Larry H. Bernstein, MD, FCAP, Curator

LPBI

 

Prions and protein-folding diseases
E. Norrby
J Intern Med 2011; 270: 1–14. http://dx.doi.org:/10.1111/j.1365-2796.2011.02387.x

Prions represent a group of proteins with a unique capacity to fold into different conformations. One isoform is rich in beta-pleated sheets and can aggregate into amyloid that may be pathogenic. This abnormal form propagates itself by imposing its confirmation on the homologous normal host cell protein. Pathogenic prions have been shown to cause lethal neurodegenerative diseases in humans and animals. These diseases are sometimes infectious and hence referred to as transmissible spongiform encephalopathies. In the present review, the remarkable evolution of the heterodox prion concept is summarized. The origin of this phenomenon is based on information transfer between homologous proteins, without the involvement of nucleic acid-encoded mechanisms. Historically, kuru and Creutzfeldt-Jakob disease (CJD) were the first infectious prion diseases to be identified in man. It was their relationship to scrapie in sheep and experimental rodents that allowed an unravelling of the particular molecular mechanism that underlie the disease process. Transmission between humans has been documented to have occurred in particular contexts, including ritual cannibalism, iatrogenic transmission because of pituitary gland-derived growth hormone or the use in neurosurgical procedures of dura mater from cadavers, and the temporary use of a prion-contaminated protein-rich feed for cows. The latter caused a major outbreak of bovine spongiform encephalopathy, which spread to man by human consumption of contaminated meat, causing approximately 200 cases of variant CJD. All these epidemics now appear to be over because of measures taken to curtail further spread of prions. Recent studies have shown that the mechanism of protein aggregation may apply to a wider range of diseases in and possibly also outside the brain, some of which are relatively common such as Alzheimer’s and Parkinson’s diseases. Furthermore, it has become apparent that the phenomenon of prion aggregation may have a wider physiological importance, but a full understanding of this remains to be defined. It may involve maintaining neuronal functions and possibly contributing to the establishment of long-term memory.

The history of the identification of the infectious nature of prion diseases and the discovery of the chemical nature of this type of infectious agent is remarkable. The great advances in this field of research have been recognized by two Nobel Prizes in Physiology or Medicine: one in 1976 to D. Carleton Gajdusek (a prize shared with Baruch S. Blumberg, for the discovery of hepatitis B virus) and the other in 1997 to Stanley B. Prusiner. Infectious prion diseases represent relatively rare phenomena mostly observed in the context of the spread of the agent by human intervention. However, the principal molecular mechanisms that lead to disease may have applications for a number of much more common noncontagious diseases. Two fundamental observations are relevant to the understanding of the molecular mechanisms involved. The first is that the same polypeptide chain, depending on the environmental conditions, including the possible presence of homologous proteins with a predetermined folding pattern, may take on dramatically altered folding. In certain cases, major aggregates of homologous proteins may be formed and such aggregates in turn may display cytopathogenic effects. A degenerative disease may ensue. The second relevant observation is that much still remains to be learnt about protein-folding phenomena and the role of information transfer systems engaging only proteins. Many proteins have sequences of amino acids that make them potentially prionogenic. Such sequences that under certain circumstances may be the cause of disease in mammals can, in another context, play a central role in physiological functions, for example, as the source of epigenetic mechanisms of protein signalling of importance for the survival of yeast cells.

In this review, our emerging understanding of the mechanisms of prion diseases will first be discussed, in particular their unique mechanisms of spread will be considered. The original belief in relatively firm barriers preventing the spread of prions between species was questioned when it became clear that bovine spongiform encephalopathy (BSE), also known as ‘mad cow disease’, could be transmitted to man. It was then shown, surprisingly, that the disease contracted from infected cattle could spread from man to man by blood transfusion. Next, the possibility of a much wider application of the pathogenic mechanism of cell destruction by protein aggregation, including degenerative processes causing for example Alzheimer’s and Parkinson’s diseases, will be discussed. The rapidly growing appreciation of the significance of signaling between proteins outside the canonical steps of the central dogma ofmolecular biology will finally be considered.  ….

Unique samples of brain collected by Gajdusek allowed identification of the histopathology of kuru. It showed many similarities to the changes in brains from patients with sporadic sCJD, but there were also similarities to the changes in brains from sheep with scrapie as noted by Hadlow [2]. His observation encouraged Gajdusek to attempt to transmit these non-inflammatory diseases to chimpanzees. He and his collaborators were successful in transmitting first kuru [3] and then CJD [4] by intracerebral inoculation of chimpanzees. The term transmissible spongiform encephalitis (TSE) was commonly used to refer to this kind of infection.

Next, after determining that kuru was infectious, the route of transmission was found to be the ritual cannibalism practiced by the Fore people [5]. The body of the deceased relative was prepared for the funeral meal, and the central nervous system containing the largest concentration of the infectious agent was consumed mainly by the women and children; thus, they were primarily affected by the disease (Fig. 1). However, no child born after 1960, the year in which the practice of ritual cannibalism ceased, has contracted kuru. The incubation time of the disease can be long, potentially longer than the life span of the individual, and cases of kuru have occurred in the present century [6]. The infectious nature of sCJD had been demonstrated, but it was initially unclear how it might spread. In fact, under normal conditions, CJD is not infectious. To date, careful studies of transfusion of blood from people incubating or even displaying early signs of CJD have not revealed any spread of the agent between individuals by this route [7]. Only under conditions of medical interventions involving brain material could an iatrogenic spread of the spontaneous form of the disease be demonstrated.

 

Throughout the 1970s, Gajdusek continued to refer to the infectious agents that cause kuru⁄CJD as slow viruses, and this situation did not change until Prusiner began to gain insights into the chemical nature of the agents using hamster scrapie as amodel to isolate and characterize them. He continued to purify the infectious material from hamster brains until he produced a relatively pure protein preparation [8]. Because of the lack of any evidence of participating nucleic acid in this preparation, he named it prion (proteinaceous and infectious particle) [9]. The protein preparation – referred to as PrP 27–30 (prion protein with a molecular weight 27–30 kD) – was pure enough to determine a short section of its amino terminal amino acid sequence. This information made it possible to determine that the gene responsible for the synthesis of the prion protein was not foreign, but a normal host cell gene [10]. Thus, it became possible to explain the absence of any inflammatory response in the tissues in the presence of this infectious disease; under healthy conditions, we do not develop immunological reactions to our own tissues.

Following the identification of the PrP gene, it was possible to produce mice deficient in PrP using ‘knockout’ technology [11]. At this time, it was known that the PrP protein appears in the brain early during embryonic development. It was found, unexpectedly, that development and life span appeared to be normal in animals without PrP protein. The PrP-knockout mice could be used for two types of critical follow-up experiments.

First, after infection with different doses of infectious prion material, the knockout mice were found to be completely refractory to development of disease [12, 13]. Furthermore, they could mount an immune response to the PrP protein, as this no longer represented an endogenous product. For the first time, antibodies could be generated against different parts of the protein. The protein that Prusiner et al. had identified was indeed critical to the pathogenic process in prion diseases.

The second type of experiment was to investigate the effects of reintroducing into the PrP-knockout mice either a modified homologous PrP gene (carrying a substitution or deletion of a single or a stretch of amino acids) or a PrP gene from a different species. The former experiment enabled attempts to dissect the role of different parts of the PrP protein in the pathogenic process (as discussed below). The latter enabled the evaluation of the species specificity of PrP proteins. Mice are normally infected only by prions from othermice or rodents, such as hamsters, but not from more distant species. However, by generation of transgenic mice carrying for example a human or a bovine PrP gene, this species barrier can be overcome providing important opportunities for studies of different kinds of pathogenic PrP proteins of relevance for human disease. Inappropriate folding and aggregation of proteins can cause disease

Diseases caused by protein aggregation have been known for a long time. They are collectively referred to as amyloid diseases, a term reflecting the original misconception that the observed stainable deposits contained starch (amylum in Latin). Later, it was demonstrated that they were in fact composed of various kinds of proteins. The amyloid deposits have characteristic staining properties and show birefringence under polarized light. Protein aggregates showing these characteristics were demonstrated in the brains of patients with CJD. However, amyloid formation is not always a feature of prion disease [14]. It is in fact found in only about 10% of the brains of patients with sCJD, but at a much higher rate in patients with other forms of the disease.

It then became possible to determine the structure of purified PrP using nuclear magnetic resonance analysis [15, 16]. It was shown that PrP can appear in two completely different forms, albeit with an identical amino acid sequence. The ‘healthy’ protein, referred to as PrP-C (control), has a structure involving predominantly two large alpha-helix structures, whereas there is a predominance of beta-pleated sheets in the pathological PrP-TSE protein (Fig. 2). It is the PrP-TSE protein that may form amyloid protein aggregates. The reason for the two completely different configurations of the same protein is not known, but a critical observation is that if a small amount of PrP-TSE is added to a larger amount of PrP-C, the ‘healthy’ protein is converted to the TSE form by an as yet undefined contagious ‘snowball’ effect. Two theoretical models, nucleation-polymerization and template assistance, have been proposed to explain this ([17], Fig. 3). However, as discussed in the next section, only certain kinds of proteins are capable of forming amyloid and are truly infectious, and the term prion is reserved for them; the term prionogenic has been introduced to include noninfectious amyloid-generating proteins.

The awareness that CJD was a disease that could be transmitted to experimental animals immediately raised the question of to what extent itmight be transmissible between humans. There was no epidemiological evidence of connections between cases of CJD, except for an increased frequency of occurrence in certain families and ethnic groups. In the light of understanding the seminal importance of PrP in the disease, it could be deduced that familial cases must be because of inherited mutations in different sites of the PrP gene, whereas sporadic cases were likely to be caused by mutation(s) accumulated in somatic (possibly brain) cells or alternatively a spontaneous emergence of amisfolded PrP protein (the nucleation– polymerization model) during the lifetime of the individual. As already mentioned, to date it has not been possible to find evidence for transmission of disease from individuals with sCJD by blood transmission [7], but relatively recent data provide evidence for a possible transmission of scrapie in sheep by experimental blood transfusion [18].

Gajdusek and collaborators at an early stage began to search for evidence of the spread of CJD through medical intervention. They found that in CJD, as in scrapie, the majority of infectious prions were located in the brain; indeed, brain tissue is about 100 000 times more infectious than peripheral tissues, such as blood [19]. The first case of iatrogenic spread of CJD between two individuals was found in connection with a corneal transplant [20], and later the similar spread to two relatively young individuals was demonstrated as a result of using electrodes for intracerebral recording [21].

Three epidemics of strikingly different origins have been documented, and all comprise slightly in excess of two hundred cases with the maximum number of cases at the end of the 1990s (Fig. 4). The first of the three epidemics was caused by the use of human growth hormone prepared from pools of many hundreds of pituitary glands from cadavers [see 19 for references]. Because these preparations were used in growing individuals, many of the victims of the disease were relatively young. When this iatrogenic spread of CJD prions was discovered, the product was rapidly withdrawn, and it was progressively replaced by growth hormone prepared by recombinant DNA technology. The average incubation time of this parenterally injected material was estimated to be 15 years (range 4–36 years). The total number of cases to date is 206, and the epidemic seems to have just reached an end. Most cases occurred in France, 109 of 1700 treated individuals. The corresponding figures are 56 of 1848 treated individuals in the UK and 28 of 7700, in the USA. In the USA, an additional step of purification was introduced in 1977, which may have reduced the risk of transmission of infectious prions.

The second epidemic has a distinctly different iatrogenic background. It relates to the previous use of heterologous cadaveric dura mater material to improve the healing process after neurosurgical interventions [see 19 for references]. The total number of cases registered to date is 196 (only 142 shown in Fig. 4), the majority (63%) of which have been in Japan. The estimated average incubation time was 11 years (range 16 months – 23 years). The use of this type of graft was banned in the UK in 1989 and in Japan in 1997. In 1987 a disinfection step with NaOH was introduced, but eventually this was not considered safe. The alternatives used today are synthetic dura mater material, connective tissue (fascia lata orfascia temporalis) from the patient or material of animal origin (bovine pericardium)’. Overall, it seems that the threat of iatrogenic spread of CJD is now minimal [19]. With the present awareness of the situation, any potential occupational risk of disease, for example, for surgeons and nurses involved in brain surgical procedures, can in practical terms be eliminated.

The main focus of interest during the last 15 years has been the third epidemic, the unexpected spread of prions from cattle to man. …..

Fig. 2 Fundamentally different structures of normal and inappropriately folded PrP protein. The latter has a predominance of beta-pleated sheets, which gives it a propensity to aggregate with other homologous proteins potentially causing destruction of tissues. Figure kindly provided by Paul Brown.

Fig. 3 Schematic model of conversion of PrP-C to PrP-TSE. In the nucleation-polymerization model, there is a rapid conversion of PrP protein between the PrP-C (circles) and PrP-TSE forms (squares), but the former is more stable. In the presence of an aggregate large enough to act as a stable nucleus, illustrated by the collection of PrP-TSE squares, a change from PrP-C to PrP-TSE is favored. In the template-assistance model, the conversion of PrP-C or a modified conformation, PrP-INT (intermediate), to Prp-TSE is extremely slow in the absence of PrP-TSE, but the process of conversion is essentially irreversible. PrP-TSE is able to propagate itself by catalysing the conversion of other PrP-INT molecules to the PrP-TSE confirmation. The final product of the two models is amyloid,which is potentially responsible for the disease process. Modified from ref. 17

In 1989 mandatory changes in slaughtering techniques were introduced. These changes ensured that the brain and spinal cord, the main sources of prions, were excluded from products used for human consumption. The precaution was taken even though at the time it was not anticipated that prions could spread from cattle directly to man, as there had never been any evidence that the scrapie agent could spread from sheep to man. In principle, the same species barrier that had prevented such a spread for hundreds of years was expected to exist also between cows andman. However, in 1994 the first case of CJD of bovine origin was identified inman [22]. For several reasons, it was concluded that this case was caused by transmission of prions from cows. ….

Once it became clear that the presence of the PrP gene was absolutely essential to the development of PrPTSE-derived diseases and that animals without PrP, unexpectedly, seemed to develop normally, it was important to determine the physiological role of the PrP protein. However, despite many studies, its fundamental function(s) still remains to be definitively identified. Different studies have highlighted a wide range of different functions [37–42]. The chromosomal gene denoted Prnp encodes PrP. It is a member of the Prn gene family, which also genes encoding two other proteins. The PrP open reading frame is encoded within a single exon directing the synthesis of a protein with 254 amino acids. This protein is post-translationally modified by removal of a 22-amino acid, amino terminal signal peptide and a 23-amino acid carboxy terminal. The latter directs the addition of a glycosylphosphatidyl inositol membrane anchor. Under normal conditions, PrP is a membrane-bound protein, but it can also show biological activity and cause infectious amyloid disease in a nonmembrane-bound form [43]. The protein has two glycosylation sites and an internal disulphide bond. All these properties are shared between molecules exerting their normal physiological function(s) and proteins causing prion diseases. The majority, but not all, PrP proteins are relatively resistant to protease digestion. This property was used in the early attempts to purify the protein. Proteinase digestion cleaves about 67 amino acids from the amino terminal of the 209-amino acid final protein product. This produces PrP 27–30, a truncated protein, which can still form amyloid. This was the protein used by Prusiner et al. to identify the nature of PrP. Alignment of PrP sequences of different mammalian origin shows a striking degree of conservation, highlighting a crucial biological function preserved through evolution [42]. However, there are also differences, which explain the species barrier to disease transmission mentioned earlier.

A number of different functions have been proposed for the normal protein: modulation of signal pathways of importance for the survival of cells, protection against oxidative stress and binding of copper. It was recently reported that membrane-bound PrP represents the major cellular receptor for the oligomeric beta-amyloid involved in Alzheimer’s disease [44]. Whether there is any significance to this possible connection between mechanisms of development of these two neurodegenerative diseases that both depend on transmission of inappropriately folded proteins remains to be seen. A number of recent studies points towards the particular importance of the PrP protein for long-term maintenance of neuronal functions. One study involving four independently targeted mouse strains depleted of PrP-C demonstrated a role of the gene product for peripheral myelin maintenance [45]. Ablation of the protein triggered chronic demyelinating neuropathy. Other recent results suggest that the seminal role of normal PrP is to maintain brain cells in good condition and protect them from overexcitement.   ….

The early studies of transmissible prion brain disease inmice and hamsters revealed that agents of different origin and⁄ or passage history could cause disease after different incubation times and with different histopathologies [51]. Originally, this was interpreted to mean that nucleic acids must play a role in prion inheritance because it was believed at the time that only this type ofmolecule could be the source of stably inherited properties. However, the more the system was analysed, the more it became clear that proteins alone could be a source of diversity, the expression of which to a considerable extent was dependent on the environmental conditions. To date, studies of hereditable human prion diseases have demonstrated correlations with more than 40 different mutations in the PrP gene [see ref 42]. These genetic variants include single-nucleotide base changes, deletions and occurrence of a varying number of segmental repeats. The effects of many of these types of genetic changes have now been mimicked by the use of transgenic mice. It has been shown that prions exist as conformationally diverse populations and that amongst these there are different strains that can replicate with independent reproducibility. Prion transformation may occur by competition and selection [52]. Other studies have focused on the effect of deletion of the part of the PrP-TSE protein that is responsible for anchoring to the cytoplasmic membrane [43]. The soluble form of PrP-TSE can still cause disease, but there is a major change in the incubation time and in histopathological changes in the infected brain [53, 54].

The propensity of certain proteins to form potentially pathogenic aggregates can be examined currently by four different approaches.

  1. Synthetic peptides exploring amino acid-dependent conformational differences that determine the emergence of polymorphic amyloid fibrils structurallymimicking prion strains.
  2. Performance of bioinformatic proteome-wide surveys for prionogenic proteins in certain species.
  3. Examination of the product(s) of replication of prions of different molecular characteristics in transgenic mice with a PrP gene construct of a preselected, potentially different species origin (possibly a chimera), with different molecular characteristics and displaying varying levels of expression.
  4. Treatment of prion inocula prior to inoculation by different procedures to attempt to increase the infectiousness of the preparation. This is referred to as in vitro generation of prions, but it should be kept in mind that the read-out of prion ‘replication’ is always anin vivo system. ….

Prion replication in mammalian systems requires the presence of both PrP-C and PrP-TSE. The latter serves as a seeding nucleus or a template onto which the physiological form of the protein is refolded into the infectious conformation (see Fig. 3). To undergo conversion, it is likely that PrP-C must develop an intermediate state.

Experimentally induced increase in the infectiousness of a prion-containing material can be achieved in vivo or in vitro. Many different experiments have demonstrated that it is the characteristics of the seeding nucleus or template that decides the nature of the final product.  ….

In further experiments, including denaturation by guanidine hydrochloride at varying concentrations, it was demonstrated that the conformational stability of the prions (either native or synthetic) correlated with the incubation period of disease [65–68]. Even protease-sensitive forms of PrP have been found to be capable of inducing disease [69].

In vitro replication of infectious PrP using a mixture in which all reagents are defined and employing a cell culture read out system as not yet been demonstrated. Nevertheless, there is general agreement that the successful generation of new infectious material that has been achieved both in vivo and in vitro rules out the possibility that prion replication is dependent on information stored in nucleic acids. ….

It has become increasingly realized that there is an extensive flow of information, or cross-talk, between proteins. Many proteins do not have a firm three-dimensional form in their native state, but represent a random coil; on coming into contact with a specific part of another protein or another chemical structure that they take on a fixed three-dimensional structure. Others can, under certain conditions, spontaneously move from secondary to tertiary and even quaternary structures. Still, protein folding as a general phenomenon has only been incompletely explained, and it is known that in many cases assisting proteins, like the chaperones, need to be present. It has been clearly demonstrated that the same polypeptide chain may take on very different conformations and that this occurs under various environmental conditions, in particular in the presence of homologous proteins already folded into one form or another. Epigenetics, i.e. the transfer of resilient genetic information not stored in nucleic acid sequences, is a rapidly expanding field and there is room for still more surprises from the study of prions.

Infectious prion diseases are rare, but the mechanism of tissue destruction by aggregation of proteins via their beta-pleated sheets seems to also apply to many other diseases, some of which are common [71, 72]. Several examples are given in Table 1. One interesting case is the beta-amyloid protein, which plays a central role in Alzheimer’s disease. …

Table 1 Prions and potential prionoids

Brain extracts from transgenic mice expressing mutant forms of tau protein have been injected into brains of other transgenic mice expressing human wild-type tau, leading to development of aggregates of the human tau [75]. Thus ‘tauopathies’ may be the result of a prion-like process in which hyperphosphorylation of the protein leads to polymerization and subsequently produces filamentous protein aggregates. There is also evidence for prion-like transmission of polyglutamine protein aggregates, characteristic of Huntington’s disease [76]. Studies have shown that amyloid protein A, the critical protein in secondary amyloidosis, injected into mouse brain can lead to degenerative disease [77]. Additional studies of material from patients with Parkinson’s disease have revealed that the occurrence of inappropriate protein folding can be transmitted from the cells of the host to transplanted cells (see [78]). Also, diseases outside the central nervous system can involve cells subjected to degenerative processes induced by inappropriately folded proteins; one example of this is diabetes type 2 [79]. Although these different diseases appear to have their origin in self-sustained aggregation of prionoid proteins, it should be noted that there is no evidence that they may be transmitted by an infectious process.

To date, the focus in studies of mammalian prions and prionogenic proteins has been on their potential for development of disease. Whether this category of proteins may also, as in the case of fungi, carry important physiological functions remains to be determined. It was recently demonstrated that the cytoplasmic polyadenylation element binding protein can form prion-like multimers in sensory neurons in the nervous system of the giant marine snail Aplysia [80]. This modification has been proposed to serve a function in long-term memory. Thus, for readers who have followed this review to the end, recollection of the salient facts and speculations presented – if stored for the future – may be due to aggregation of prionogenic proteins in the brain, provided of course that the fundamental long-term memory mechanisms of the human brain are similar to those of Aplysia.

 

Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution
Massimo Stefani · Christopher M. Dobson
J Mol Med 2003; 81:678–699      http://dx.doi.org:/10.1007/s00109-003-0464-5

The deposition of proteins in the form of amyloid fibrils and plaques is the characteristic feature of more than 20 degenerative conditions affecting either the central nervous system or a variety of peripheral tissues. As these conditions include Alzheimer’s, Parkinson’s and the prion diseases, several forms of fatal systemic amyloidosis, and at least one condition associated with medical intervention (haemodialysis), they are of enormous importance in the context of present-day human health and welfare. Much remains to be learned about the mechanism by which the proteins associated with these diseases aggregate and form amyloid structures, and how the latter affect the functions of the organs with which they are associated. A great deal of information concerning these diseases has emerged, however, during the past 5 years, much of it causing a number of fundamental assumptions about the amyloid diseases to be reexamined. For example, it is now apparent that the ability to form amyloid structures is not an unusual feature of the small number of proteins associated with these diseases but is instead a general property of polypeptide chains. It has also been found recently that aggregates of proteins not associated with amyloid diseases can impair the ability of cells to function to a similar extent as aggregates of proteins linked with specific neurodegenerative conditions. Moreover, the mature amyloid fibrils or plaques appear to be substantially less toxic than the prefibrillar aggregates that are their precursors. The toxicity of these early aggregates appears to result from an intrinsic ability to impair fundamental cellular processes by interacting with cellular membranes, causing oxidative stress and increases in free Ca2+ that eventually lead to apoptotic or necrotic cell death. The ‘new view’ of these diseases also suggests that other degenerative conditions could have similar underlying origins to those of the amyloidoses. In addition, cellular protection mechanisms, such as molecular chaperones and the protein degradation machinery, appear to be crucial in the prevention of disease in normally functioning living organisms. It also suggests some intriguing new factors that could be of great significance in the evolution of biological molecules and the mechanisms that regulate their behavior.

The genetic information within a cell encodes not only the specific structures and functions of proteins but also the way these structures are attained through the process known as protein folding. In recent years many of the underlying features of the fundamental mechanism of this complex process and the manner in which it is regulated in living systems have emerged from a combination of experimental and theoretical studies [1]. The knowledge gained from these studies has also raised a host of interesting issues. It has become apparent, for example, that the folding and unfolding of proteins is associated with a whole range of cellular processes from the trafficking of molecules to specific organelles to the regulation of the cell cycle and the immune response. Such observations led to the inevitable conclusion that the failure to fold correctly, or to remain correctly folded, gives rise to many different types of biological malfunctions and hence to many different forms of disease [2]. In addition, it has been recognised recently that a large number of eukaryotic genes code for proteins that appear to be ‘natively unfolded’, and that proteins can adopt, under certain circumstances, highly organised multi-molecular assemblies whose structures are not specifically encoded in the amino acid sequence. Both these observations have raised challenging questions about one of the most fundamental principles of biology: the close relationship between the sequence, structure and function of proteins, as we discuss below [3]. It is well established that proteins that are ‘misfolded’, i.e. that are not in their functionally relevant conformation, are devoid of normal biological activity. In addition, they often aggregate and/or interact inappropriately with other cellular components leading to impairment of cell viability and eventually to cell death. Many diseases, often known as misfolding or conformational diseases, ultimately result from the presence in a living system of protein molecules with structures that are ‘incorrect’, i.e. that differ from those in normally functioning organisms [4]. Such diseases include conditions in which a specific protein, or protein complex, fails to fold correctly (e.g. cystic fibrosis, Marfan syndrome, amyotonic lateral sclerosis) or is not sufficiently stable to perform its normal function (e.g. many forms of cancer). They also include conditions in which aberrant folding behaviour results in the failure of a protein to be correctly trafficked (e.g. familial hypercholesterolaemia, α1-antitrypsin deficiency, and some forms of retinitis pigmentosa) [4]. The tendency of proteins to aggregate, often to give species extremely intractable to dissolution and refolding, is of course also well known in other circumstances. Examples include the formation of inclusion bodies during overexpression of heterologous proteins in bacteria and the precipitation of proteins during laboratory purification procedures. Indeed, protein aggregation is well established as one of the major difficulties associated with the production and handling of proteins in the biotechnology and pharmaceutical industries [5].

Considerable attention is presently focused on a group of protein folding diseases known as amyloidoses. In these diseases specific peptides or proteins fail to fold or to remain correctly folded and then aggregate (often with other components) so as to give rise to ‘amyloid’ deposits in tissue. Amyloid structures can be recognised because they possess a series of specific tinctorial and biophysical characteristics that reflect a common core structure based on the presence of highly organised β- sheets [6]. The deposits in strictly defined amyloidoses are extracellular and can often be observed as thread-like fibrillar structures, sometimes assembled further into larger aggregates or plaques. These diseases include a range of sporadic, familial or transmissible degenerative diseases, some of which affect the brain and the central nervous system (e.g. Alzheimer’s and Creutzfeldt-Jakob diseases), while others involve peripheral tissues and organs such as the liver, heart and spleen (e.g. systemic amyloidoses and type II diabetes) [7, 8]. In other forms of amyloidosis, such as primary or secondary systemic amyloidoses, proteinaceous deposits are found in skeletal tissue and joints (e.g. haemodialysis-related amyloidosis) as well as in several organs (e.g. heart and kidney). Yet other components such as collagen, glycosaminoglycans and proteins (e.g. serum amyloid protein) are often present in the deposits protecting them against degradation [9, 10, 11]. Similar deposits to those in the amyloidoses are, however, found intracellularly in other diseases; these can be localised either in the cytoplasm, in the form of specialised aggregates known as aggresomes or as Lewy or Russell bodies or in the nucleus (see below).

The presence in tissue of proteinaceous deposits is a hallmark of all these diseases, suggesting a causative link between aggregate formation and pathological symptoms (often known as the amyloid hypothesis) [7, 8, 12]. At the present time the link between amyloid formation and disease is widely accepted on the basis of a large number of biochemical and genetic studies. The specific nature of the pathogenic species, and the molecular basis of their ability to damage cells, are however, the subject of intense debate [13, 14, 15, 16, 17, 18, 19, 20]. In neurodegenerative disorders it is very likely that the impairment of cellular function follows directly from the interactions of the aggregated proteins with cellular components [21, 22]. In the systemic non-neurological diseases, however, it is widely believed that the accumulation in vital organs of large amounts of amyloid deposits can by itself cause at least some of the clinical symptoms [23]. It is quite possible, however, that there are other more specific effects of aggregates on biochemical processes even in these diseases. The presence of extracellular or intracellular aggregates of a specific polypep tide molecule is a characteristic of all the 20 or so recognised amyloid diseases. The polypeptides involved include full length proteins (e.g. lysozyme or immunoglobulin light chains), biological peptides (amylin, atrial natriuretic factor) and fragments of larger proteins produced as a result of specific processing (e.g. the Alzheimer β- peptide) or of more general degradation [e.g. poly(Q) stretches cleaved from proteins with poly(Q) extensions such as huntingtin, ataxins and the androgen receptor]. The peptides and proteins associated with known amyloid diseases are listed in Table 1. In some cases the proteins involved have wild type sequences, as in sporadic forms of the diseases, but in other cases these are variants resulting from genetic mutations associated with familial forms of the diseases. In some cases both sporadic and familial diseases are associated with a given protein; in this case the mutational variants are usually associated with early-onset forms of the disease. In the case of the neurodegenerative diseases associated with the prion protein some forms of the diseases are transmissible. The existence of familial forms of a number of amyloid diseases has provided significant clues to the origins of the pathologies. For example, there are increasingly strong links between the age at onset of familial forms of disease and the effects of the mutations involved on the propensity of the affected proteins to aggregate in vitro. Such findings also support the link between the process of aggregation and the clinical manifestations of disease [24, 25].

The presence in cells of misfolded or aggregated proteins triggers a complex biological response. In the cytosol, this is referred to as the ‘heat shock response’ and in the endoplasmic reticulum (ER) it is known as the ‘unfolded protein response’. These responses lead to the expression, among others, of the genes for heat shock proteins (Hsp, or molecular chaperone proteins) and proteins involved in the ubiquitin-proteasome pathway [26]. The evolution of such complex biochemical machinery testifies to the fact that it is necessary for cells to isolate and clear rapidly and efficiently any unfolded or incorrectly folded protein as soon as it appears. In itself this fact suggests that these species could have a generally adverse effect on cellular components and cell viability. Indeed, it was a major step forward in understanding many aspects of cell biology when it was recognised that proteins previously associated only with stress, such as heat shock, are in fact crucial in the normal functioning of living systems. This advance, for example, led to the discovery of the role of molecular chaperones in protein folding and in the normal ‘housekeeping’ processes that are inherent in healthy cells [27, 28]. More recently a number of degenerative diseases, both neurological and systemic, have been linked to, or shown to be affected by, impairment of the ubiquitin-proteasome pathway (Table 2). The diseases are primarily associated with a reduction in either the expression or the biological activity of Hsps, ubiquitin, ubiquitinating or deubiquitinating enzymes and the proteasome itself, as we show below [29, 30, 31, 32], or even to the failure of the quality control mechanisms that ensure proper maturation of proteins in the ER. The latter normally leads to degradation of a significant proportion of polypeptide chains before they have attained their native conformations through retrograde translocation to the cytosol [33, 34]. For example, the most common mutation of the CFTR chloride channel associated with cystic fibrosis interferes with the cor rect folding of the polypeptide chain; as a consequence, much of the mutated protein is not secreted but is retained in the ER and rapidly degraded even though, when properly folded, it could still function as ion channel at the cell surface ([35] and references therein).

Table 1 A summary of the main amyloidoses and the proteins or peptides involved

Table 2 Neurodegenerative diseases with inclusion bodies shown to be linked to deficits of the ubiquitin-proteasome pathway (modified from [26])

It is now well established that the molecular basis of protein aggregation into amyloid structures involves the existence of ‘misfolded’ forms of proteins, i.e. proteins that are not in the structures in which they normally function in vivo or of fragments of proteins resulting from degradation processes that are inherently unable to fold [4, 7, 8, 36]. Aggregation is one of the common consequences of a polypeptide chain failing to reach or maintain its functional three-dimensional structure. Such events can be associated with specific mutations, misprocessing phenomena, aberrant interactions with metal ions, changes in environmental conditions, such as pH or temperature, or chemical modification (oxidation, proteolysis). Perturbations in the conformational properties of the polypeptide chain resulting from such phenomena may affect equilibrium 1 in Fig. 1 increasing the population of partially unfolded, or misfolded, species that are much more aggregation-prone than the native state. …

Fig. 1 Overview of the possible fates of a newly synthesised polypeptide chain. The equilibrium ① between the partially folded molecules and the natively folded ones is usually strongly in favour of the latter except as a result of specific mutations, chemical modifications or partially destabilising solution conditions. The increased equilibrium populations of molecules in the partially or completely unfolded ensemble of structures are usually degraded by the proteasome; when this clearance mechanism is impaired, such species often form disordered aggregates or shift equilibrium ② towards the nucleation of pre-fibrillar assemblies that eventually grow into mature fibrils (equilibrium ③). DANGER! indicates that pre-fibrillar aggregates in most cases display much higher toxicity than mature fibrils. Heat shock proteins (Hsp) can suppress the appearance of pre-fibrillar assemblies by minimising the population of the partially folded molecules by assisting in the correct folding of the nascent chain and the unfolded protein response target incorrectly folded proteins for degradation.

The various peptides and proteins associated with amyloid diseases have no obvious similarities in size, amino acid composition, sequence or structure. Nevertheless, the amyloid fibrils into which they convert have marked similarities both in their external morphology (Fig. 2) and in their internal structure (Fig. 3). Circular dichroism and Fourier transform infra-red spectroscopy both indicate a high content of β-structure, even when the monomeric peptide or protein is substantially disordered or rich in α-helical structure. Although it has not yet proved possible to obtain a detailed definition of the molecular structure of any amyloid fibril, investigations by electron and atomic force microscopy show that they are typically long, straight and unbranched. The fibrils are typically 6–12 nm in diameter and usually consist of two to six ‘protofilaments’, each of diameter about 2 nm, that are often twisted around each other to form supercoiled rope-like structures [38, 39]. Each protofilament in such structures appears to have a highly ordered inner core that X-ray fibre diffraction data suggest consists of some or all of the polypeptide chain arranged in a characteristic cross-β structure. In this structural organisation, the β-strands run perpendicular to the protofilament axis, resulting in a series of β-sheets that propagate along the direction of the fibril (Fig. 3).

Little is known at present about the detailed arrangement of the polypeptide chains themselves within amyloid fibrils, either those parts involved in the core β- strands or in regions that connect the various β-strands. Recent data suggest that the sheets are relatively untwisted and may in some cases at least exist in quite specific supersecondary structure motifs such as β-helices [6, 40] or the recently proposed µ-helix [41]. It seems possible that there may be significant differences in the way the strands are assembled depending on characteristics of the polypeptide chain involved [6, 42]. Factors including length, sequence (and in some cases the presence of disulphide bonds or post-translational modifications such as glycosylation) may be important in determining details of the structures. Several recent papers report structural models for amyloid fibrils containing different polypeptide chains, including the Aβ40 peptide, insulin and fragments of the prion protein, based on data from such techniques as cryo-electron microscopy and solid-state magnetic resonance spectroscopy [43, 44]. These models have much in common and do indeed appear to reflect the fact that the structures of different fibrils are likely to be variations on a common theme [40]. It is also emerging that there may be some common and highly organised assemblies of amyloid protofilaments that are not simply extended threads or ribbons. It is clear, for example, that in some cases large closed loops can be formed [45, 46, 47], and there may be specific types of relatively small spherical or ‘doughnut’ shaped structures that can result in at least some circumstances.

Fig. 4 Some amyloid-related peptides/proteins form early aggregates of globular appearance that further organise into beaded chains, globular annular ‘doughnut’ shaped assemblies eventually giving mature protofilaments and fibrils. Pre-fibrilar aggregates may interact with reconstituted phospholipid membranes and with cell membranes where they form aspecific channels (pores) disrupting cellular homeostasis. The latter possible mechanism of toxicity is similar to that displayed by antimicrobial peptides, pore-forming eukaryotic proteins and bacterial toxins and newly synthesised cyclic peptide antibiotics (see text). The electron micrographs of the globular and beaded chains of Aβ peptides are taken from Harper et al. [200]. The electron micrographs of the rings of the α-synuclein A53T (upper row) and A30P (middle row) mutants and of the Alzheimer precursor protein artic mutant (lower row) are from [201].

The similarity of some early amyloid aggregates with the pores resulting from oligomerisation of bacterial toxins and pore-forming eukaryotic proteins (see below) also suggest that the basic mechanism of protein aggregation into amyloid structures may not only be associated with diseases but in some cases could result in species with functional significance. Recent evidence indicates that a variety of micro-organisms may exploit the controlled aggregation of specific proteins (or their precursors) to generate functional structures. Examples include bacterial curli [52] and proteins of the interior fibre cells of mammalian ocular lenses, whose β-sheet arrays seem to be organised in an amyloid-like supramolecular order [53]. In this case the inherent stability of amyloid-like protein structure may contribute to the long-term structural integrity and transparency of the lens. Recently it has been hypothesised that amyloid-like aggregates of serum amyloid A found in secondary amyloidoses following chronic inflammatory diseases protect the host against bacterial infections by inducing lysis of bacterial cells [54]. One particularly interesting example is a ‘misfolded’ form of the milk protein α-lactalbumin that is formed at low pH and trapped by the presence of specific lipid molecules [55]. This form of the protein has been reported to trigger apoptosis selectively in tumour cells providing evidence for its importance in protecting infants from certain types of cancer [55]. ….

Until about 30 years ago proteolysis was considered to be the primary factor triggering the formation of amyloid aggregates in vivo, following the demonstration that lysosomal enzymes, at acidic pH values, are able to convert amyloidogenic proteins into amyloid fibrils [56]. This idea was challenged around 10 years ago when it was shown that transthyretin can be converted in vitro into amyloid fibrils following an acid-induced conformational change [57]. This finding demonstrated that a modification of the three-dimensional structure was sufficient to enable the production of an aggregation-prone species. This suggestion was not immediately accepted, at least in part as a consequence of the well established fact that the peptide found in the plaques characteristic of Alzheimer’s disease resulted from proteolysis of the Alzheimer’s precursor protein. Following these initial observations a large number of proteins known to aggregate in vivo were found to form fibrillar aggregates in vitro as a result of induced conformational changes; these data, however, reinforced the idea that the molecular basis of protein aggregation was an unusual feature of the few peptides and proteins found to be associated with the amyloid diseases, resulting from a specific conformational change related to the specific amino acid sequences. In 1998 two papers were published, each reporting the observation that a protein unrelated to any amyloid disease aggregated in vitro to form structures indistinguishable from the amyloid fibrils that could be produced from the disease-associated peptides and proteins [58, 59]. These observations were made by chance, but it was soon shown that a similar conversion could be achieved deliberately for other proteins by a rational choice of solution conditions [60, 61]. Since then a substantial number of similar studies have been reported ([61] and references therein; Table 3). In each case aggregation of a full-length protein to form amyloid fibrils was found to require solution conditions (such as low pH, lack of specific ligands, high temperature, moderate concentrations of salts or co-solvents such as trifluoroethanol) such that the native structure was partially or completely disrupted but under which interactions such as hydrogen-bonding were not completely inhibited. …..

It was generally assumed until recently that the proteinaceous aggregates most toxic to cells are likely to be mature amyloid fibrils, the form of aggregates that have been commonly detected in pathological deposits. It therefore appeared probable that the pathogenic features underlying amyloid diseases are a consequence of the interaction with cells of extracellular deposits of aggregated material. As well as forming the basis for understanding the fundamental causes of these diseases, this scenario stimulated the exploration of therapeutic approaches to amyloidoses that focused mainly on the search for molecules able to impair the growth and deposition of fibrillar forms of aggregated proteins. An increasing quantity of recent experimental data suggests, however, that in many cases at least the species that are most highly toxic to cells are the pre-fibrillar aggregates (sometimes referred to as amorphous aggregates, protein micelles or protofibrils) rather than the mature fibrils into which they often develop. In particular, a number of reports concerning Aβ peptides, α synuclein and transthyretin indicate that these early aggregates are the most toxic species [18, 76, 77, 78, 79, 80]; in addition, the presence of such species has also been reported for huntingtin [44], and possibly the androgen receptor [81] in diseased transgenic mice. The hypothesis that toxicity is exhibited primarily by early aggregates also provides an explanation for the lack of existence of a direct correlation between the density of fibrillar plaques in the brains of victims of Alzheimer’s disease and the severity of the clinical symptoms [82]. ….

The presence of toxic aggregates inside or outside cells can impair a number of cell functions that ultimately lead to cell death by an apoptotic mechanism [95, 96]. Recent research suggests, however, that in most cases initial perturbations to fundamental cellular processes underlie the impairment of cell function induced by aggregates of disease-associated polypeptides. Many pieces of data point to a central role of modifications to the intracellular redox status and free Ca2+ levels in cells exposed to toxic aggregates [45, 89, 97, 98, 99, 100, 101]. A modification of the intracellular redox status in such cells is associated with a sharp increase in the quantity of reactive oxygen species (ROS) that is reminiscent of the oxidative burst by which leukocytes destroy invading foreign cells after phagocytosis. In addition, changes have been observed in reactive nitrogen species, lipid peroxidation, deregulation of NO metabolism [97], protein nitrosylation [102] and upregulation of heme oxygenase-1, a specific marker of oxidative stress [103]. …..

It is not clear why protein aggregation is followed, even in vitro, by production of ROS. In the case of Aβ42, Met35, Gly29 and Gly33 have been suggested to be involved [109]; a role has also been proposed for metal ions such as Fe, Cu and Zn, for example, through the generation of hydroxide radicals from hydrogen peroxide [110, 111]. An upregulation of the activity of hydrogen peroxide-producing membrane enzymes, such as plasma membrane NADPH oxidase and ER cytochrome P450 reductase, has also been reported in Aβ-induced neurotoxicity in microglia and in cortical neurons [112, 113]. More generally, intracellular oxidative stress could be related to some form of destabilisation of cell membranes by toxic species leading to a failure to regulate appropriately plasma membrane proteins such as receptors and ion pumps [114] and/or to impairment of mitochondrial function. Mitochondria play a well recognised role in oxidative stress and apoptosis; in this regard, a key factor in Aβ peptide neurotoxicity could be the opening of mitochondrial permeability transition pores by Ca2+ entry in neuronal mitochondria [115] followed by release of cytochrome c, a strong inducer of apoptosis. …

Since 1993, a ‘channel hypothesis’ of the molecular basis of the cytotoxicity of amyloid aggregates has been put forward [131] by similarity with the proposed mechanism of toxicity of pore-forming peptides and proteins [90, 91]. As is pointed out above, this idea stems from a number of pieces of evidence leading to the proposal that unchaperoned, positively charged and misfolded proteins, or early aggregates of such species, can interact with lipid membranes ([90, 91] and references therein). Evidence for this proposal comes from the study of both artificial model systems, such as phospholipid bilayers, and cell membranes; in the latter the function of specific membrane proteins has been found to be impaired [78, 91]. In most cases interaction of a misfolded species with a membrane would occur via a two-step mechanism involving electrostatic interaction of the positively charged residues with negatively charged or polar lipid head groups followed by the insertion of hydrophobic regions into the membrane hydrophobic interior [91].

According to this hypothesis, misfolding of proteins, such as at least some of those involved in neurodegenerative diseases, would then induce cytotoxicity. Such cytotoxicity would be a direct consequence of the exposure of hydrophobic regions, favouring the interaction of the misfolded species with the plasma membrane and other cell membranes and leading to membrane damage via the formation of non-specific ion channels. These channels, or pores, have been described for a number of peptide and proteins associated with amyloid disease including Aβ peptides [19, 45, 78, 89] and their fragments [132], α-synuclein [133], islet-amyloid polypeptide [86], the 106–126 fragment of the prion protein [41], poly(Q) stretches [134, 135], the C-type natriuretic peptide [84], β2-microglobulin [48], transthyretin [136], murine serum amyloid A [137] and the N-terminal peptide of an acutephase isoform variant of human serum amyloid A1.1 (SAAp) [54]. The channels have been investigated primarily by recording ion currents across biological or reconstituted membranes, but ‘doughnuts’ of channel-like assemblies of pre-fibrillar aggregates of Aβ1–42, α-synuclein, transthyretin and serum amyloid A have also been observed by electron and atomic force microscopy [45, 46, 49, 137]. ….

In general, heterogeneity of amyloid intermediates, including globules, chains, doughnuts, protofilaments and fibrils, could result in increased potency of toxicity since the different types of intermediates may act in differing ways on membranes such as the suite of peptides in venoms. In the case of α-synuclein the ‘pores’ coexist with fibrils under conditions of molecular crowding [138], raising the possibility that the former are more stable under cytoplasmic conditions and leading to the proposal that they are the pathogenic species in Parkinson’s disease [46]. The size-dependent permeabilisation of artificial vesicles by protofibrillar α-synuclein suggests that permeabilisation occurs mainly as a result of a specific membrane perturbation via the formation of pores at least 2.5 nm in diameter [46]. If α-synuclein annular protofibrils are the pathogenic species in Parkinson’s disease and other amyloidoses, inhibition of their production should represent a suitable therapeutic strategy. However, it is difficult to imagine a drug molecule able to distinguish specifically among chain protofibrils, annular protofibrils and mature fibrils, when one considers that protofibril elongation into fibrils and protofibril annulation are likely to involve the same interactions leading to β-sheet extension [88]. ….

Fig. 6 Flow-chart of the main molecular steps leading misfolded polypeptide chains to induce cell death. In the panel, aggregation of proteins into fully formed, mature amyloid fibrils could be considered to be potentially beneficial in the light of recent findings indicating that, at least in most cases, the true toxic species are the early pre-fibrillar aggregates, whereas mature fibrils appear less toxic or devoid of toxicity. Degradation of misfolded proteins is carried out by the ubiquitin-proteasome machinery. The path leading to cell death occurs when the chaperone and clearing cellular machineries are overwhelmed by the presence of an excess of unfolded/malfolded proteins; the latter is followed by the appearance of unstable amyloid nuclei and pre-fibrillar assemblies further growing into mature fibrils; such assemblies may also interact with cell membranes destabilising them and modifying ion balance possibly by formation of aspecific membrane pores. The rise of the intracellular free Ca2+ and ROS is one of the earliest modification in the path of cell death following cell exposure to early amyloid aggregates of most peptides and proteins. (Modified from [91]).

The potential cytotoxicity of many aggregated proteins suggests that, in addition to providing cells with mechanisms to clear unfolded and misfolded proteins and to minimise their ability to induce toxicity, evolution must also have operated to eliminate protein sequences with a high intrinsic propensity to aggregate [8]. Thus mutations that are neutral with respect to protein function could be selected against because they enhance the tendency of proteins to aggregate under physiological conditions. It is interesting in this regard that most of the polypeptide chains associated with aggregation diseases are either intact, or fragments of, proteins that are secreted or membrane bound. It could be that such proteins are more easily able to escape the cellular mechanisms that protect against misfolding and aggregation. Moreover, it is possible that processing in the ER prior to secretion through the Golgi, or indeed the events involved in the retrograde translocation into the cytosol of polypeptide chains that have failed the quality-control tests in the ER [35], represent additional steps associated with folding in which errors could occur or accumulate. The recent studies of the ways in which structural adaptations of proteins can minimise their tendency to misfold and aggregate mentioned above show, however, that polypeptides are far from optimised in their ability to resist aggregation. One reason for this fact is that sequences must encode many features of proteins, such as their need to fold and to bind to other species. Another is that sequences selected by evolution are in general optimised only to an extent that allows a particular organism to function efficiently during its normal life span [148]. …

The data reported in the past few years strongly suggest that the conversion of normally soluble proteins into amyloid fibrils and the toxicity of small aggregates appearing during the early stages of the formation of the latter are common or generic features of polypeptide chains. Moreover, the molecular basis of this toxicity also appears to display common features between the different systems that have so far been studied. The ability of many, perhaps all, natural polypeptides to ‘misfold’ and convert into toxic aggregates under suitable conditions suggests that one of the most important driving forces in the evolution of proteins must have been the negative selection against sequence changes that increase the tendency of a polypeptide chain to aggregate. Nevertheless, as protein folding is a stochastic process, and no such process can be completely infallible, misfolded proteins or protein folding intermediates in equilibrium with the natively folded molecules must continuously form within cells. Thus mechanisms to deal with such species must have co-evolved with proteins. Indeed, it is clear that misfolding, and the associated tendency to aggregate, is kept under control by molecular chaperones, which render the resulting species harmless assisting in their refolding, or triggering their degradation by the cellular clearance machinery [166, 167, 168, 169, 170, 171, 172, 173, 175, 177, 178]. Misfolded and aggregated species are likely to owe their toxicity to the exposure on their surfaces of regions of proteins that are buried in the interior of the structures of the correctly folded native states. The exposure of large patches of hydrophobic groups is likely to be particularly significant as such patches favour the interaction of the misfolded species with cell membranes [44, 83, 89, 90, 91, 93]. Interactions of this type are likely to lead to the impairment of the function and integrity of the membranes involved, giving rise to a loss of regulation of the intracellular ion balance and redox status and eventually to cell death. In addition, misfolded proteins undoubtedly interact inappropriately with other cellular components, potentially giving rise to the impairment of a range of other biological processes. Under some conditions the intracellular content of aggregated species may increase directly, due to an enhanced propensity of incompletely folded or misfolded species to aggregate within the cell itself. This could occur as the result of the expression of mutational variants of proteins with decreased stability or cooperativity or with an intrinsically higher propensity to aggregate. It could also occur as a result of the overproduction of some types of protein, for example, because of other genetic factors or other disease conditions, or because of perturbations to the cellular environment that generate conditions favouring aggregation, such as heat shock or oxidative stress. Finally, the accumulation of misfolded or aggregated proteins could arise from the chaperone and clearance mechanisms becoming overwhelmed as a result of specific mutant phenotypes or of the general effects of ageing [173, 174].

The topics discussed in this review not only provide a great deal of evidence for the ‘new view’ that proteins have an intrinsic capability of misfolding and forming structures such as amyloid fibrils but also suggest that the role of molecular chaperones is even more important than was thought in the past. The role of these ubiquitous proteins in enhancing the efficiency of protein folding is well established [185]. It could well be that they are at least as important in controlling the harmful effects of misfolded or aggregated proteins as in enhancing the yield of functional molecules.
https://www.researchgate.net/profile/Massimo_Stefani/publication/10595052_Protein_Aggregation_and_Aggregate_Toxicity_New_Insights_into_Protein_Folding_Misfolding_Diseases_and_Biological_Evolution/links/0046352171a742f19a000000.pdf

 

Protein Misfolding, Evolution and Disease
Dobson C. M.
Trends in biochemical sciences 1999; 24(9): 329-332   0968-0004
http://www.ncbi.nlm.nih.gov/pubmed/10470028
http://dx.doi.org/10.1016/S0968-0004(99)01445-0

 

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CRISPR/Cas9, Familial Amyloid Polyneuropathy ( FAP) and Neurodegenerative Disease

CRISPR/Cas9, Familial Amyloid Polyneuropathy (FAP) and Neurodegenerative Disease, Volume 2 (Volume Two: Latest in Genomics Methodologies for Therapeutics: Gene Editing, NGS and BioInformatics, Simulations and the Genome Ontology), Part 2: CRISPR for Gene Editing and DNA Repair

CRISPR/Cas9, Familial Amyloid Polyneuropathy ( FAP) and Neurodegenerative Disease

Curator: Larry H. Bernstein, MD, FCAP

 

CRISPR/Cas9 and Targeted Genome Editing: A New Era in Molecular Biology

https://www.neb.com/tools-and-resources/feature-articles/crispr-cas9-and-targeted-genome-editing-a-new-era-in-molecular-biology

The development of efficient and reliable ways to make precise, targeted changes to the genome of living cells is a long-standing goal for biomedical researchers. Recently, a new tool based on a bacterial CRISPR-associated protein-9 nuclease (Cas9) from Streptococcus pyogenes has generated considerable excitement (1). This follows several attempts over the years to manipulate gene function, including homologous recombination (2) and RNA interference (RNAi) (3). RNAi, in particular, became a laboratory staple enabling inexpensive and high-throughput interrogation of gene function (4, 5), but it is hampered by providing only temporary inhibition of gene function and unpredictable off-target effects (6). Other recent approaches to targeted genome modification – zinc-finger nucleases [ZFNs, (7)] and transcription-activator like effector nucleases [TALENs (8)]– enable researchers to generate permanent mutations by introducing doublestranded breaks to activate repair pathways. These approaches are costly and time-consuming to engineer, limiting their widespread use, particularly for large scale, high-throughput studies.

The Biology of Cas9

The functions of CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats) and CRISPR-associated (Cas) genes are essential in adaptive immunity in select bacteria and archaea, enabling the organisms to respond to and eliminate invading genetic material. These repeats were initially discovered in the 1980s in E. coli (9), but their function wasn’t confirmed until 2007 by Barrangou and colleagues, who demonstrated that S. thermophilus can acquire resistance against a bacteriophage by integrating a genome fragment of an infectious virus into its CRISPR locus (10).

Three types of CRISPR mechanisms have been identified, of which type II is the most studied. In this case, invading DNA from viruses or plasmids is cut into small fragments and incorporated into a CRISPR locus amidst a series of short repeats (around 20 bps). The loci are transcribed, and transcripts are then processed to generate small RNAs (crRNA – CRISPR RNA), which are used to guide effector endonucleases that target invading DNA based on sequence complementarity (Figure 1) (11).

Figure 1. Cas9 in vivo: Bacterial Adaptive Immunity

https://www.neb.com/~/media/NebUs/Files/Feature%20Articles/Images/FA_Cas9_Fig1_Cas9InVivo.png

In the acquisition phase, foreign DNA is incorporated into the bacterial genome at the CRISPR loci. CRISPR loci is then transcribed and processed into crRNA during crRNA biogenesis. During interference, Cas9 endonuclease complexed with a crRNA and separate tracrRNA cleaves foreign DNA containing a 20-nucleotide crRNA complementary sequence adjacent to the PAM sequence. (Figure not drawn to scale.)

https://www.neb.com/~/media/NebUs/Files/Feature%20Articles/Images/FA_Cas9_GenomeEditingGlossary.png

One Cas protein, Cas9 (also known as Csn1), has been shown, through knockdown and rescue experiments to be a key player in certain CRISPR mechanisms (specifically type II CRISPR systems). The type II CRISPR mechanism is unique compared to other CRISPR systems, as only one Cas protein (Cas9) is required for gene silencing (12). In type II systems, Cas9 participates in the processing of crRNAs (12), and is responsible for the destruction of the target DNA (11). Cas9’s function in both of these steps relies on the presence of two nuclease domains, a RuvC-like nuclease domain located at the amino terminus and a HNH-like nuclease domain that resides in the mid-region of the protein (13).

To achieve site-specific DNA recognition and cleavage, Cas9 must be complexed with both a crRNA and a separate trans-activating crRNA (tracrRNA or trRNA), that is partially complementary to the crRNA (11). The tracrRNA is required for crRNA maturation from a primary transcript encoding multiple pre-crRNAs. This occurs in the presence of RNase III and Cas9 (12).

During the destruction of target DNA, the HNH and RuvC-like nuclease domains cut both DNA strands, generating double-stranded breaks (DSBs) at sites defined by a 20-nucleotide target sequence within an associated crRNA transcript (11, 14). The HNH domain cleaves the complementary strand, while the RuvC domain cleaves the noncomplementary strand.

The double-stranded endonuclease activity of Cas9 also requires that a short conserved sequence, (2–5 nts) known as protospacer-associated motif (PAM), follows immediately 3´- of the crRNA complementary sequence (15). In fact, even fully complementary sequences are ignored by Cas9-RNA in the absence of a PAM sequence (16).

Cas9 and CRISPR as a New Tool in Molecular Biology

The simplicity of the type II CRISPR nuclease, with only three required components (Cas9 along with the crRNA and trRNA) makes this system amenable to adaptation for genome editing. This potential was realized in 2012 by the Doudna and Charpentier labs (11). Based on the type II CRISPR system described previously, the authors developed a simplified two-component system by combining trRNA and crRNA into a single synthetic single guide RNA (sgRNA). sgRNAprogrammed Cas9 was shown to be as effective as Cas9 programmed with separate trRNA and crRNA in guiding targeted gene alterations (Figure 2A).

To date, three different variants of the Cas9 nuclease have been adopted in genome-editing protocols. The first is wild-type Cas9, which can site-specifically cleave double-stranded DNA, resulting in the activation of the doublestrand break (DSB) repair machinery. DSBs can be repaired by the cellular Non-Homologous End Joining (NHEJ) pathway (17), resulting in insertions and/or deletions (indels) which disrupt the targeted locus. Alternatively, if a donor template with homology to the targeted locus is supplied, the DSB may be repaired by the homology-directed repair (HDR) pathway allowing for precise replacement mutations to be made (Figure 2A) (17, 18).

Cong and colleagues (1) took the Cas9 system a step further towards increased precision by developing a mutant form, known as Cas9D10A, with only nickase activity. This means it cleaves only one DNA strand, and does not activate NHEJ. Instead, when provided with a homologous repair template, DNA repairs are conducted via the high-fidelity HDR pathway only, resulting in reduced indel mutations (1, 11, 19). Cas9D10A is even more appealing in terms of target specificity when loci are targeted by paired Cas9 complexes designed to generate adjacent DNA nicks (20) (see further details about “paired nickases” in Figure 2B).

The third variant is a nuclease-deficient Cas9 (dCas9, Figure 2C) (21). Mutations H840A in the HNH domain and D10A in the RuvC domain inactivate cleavage activity, but do not prevent DNA binding (11, 22). Therefore, this variant can be used to sequence-specifically target any region of the genome without cleavage. Instead, by fusing with various effector domains, dCas9 can be used either as a gene silencing or activation tool (21, 23–26). Furthermore, it can be used as a visualization tool. For instance, Chen and colleagues used dCas9 fused to Enhanced Green Fluorescent Protein (EGFP) to visualize repetitive DNA sequences with a single sgRNA or nonrepetitive loci using multiple sgRNAs (27).

Figure 2. CRISPR/Cas9 System Applications

https://www.neb.com/~/media/NebUs/Files/Feature%20Articles/Images/FA_Cas9_Fig2_Cas9forGenomeEditing.png?device=modal

  1. Wild-type Cas9 nuclease site specifically cleaves double-stranded DNA activating double-strand break repair machinery. In the absence of a homologous repair template non-homologous end joining can result in indels disrupting the target sequence. Alternatively, precise mutations and knock-ins can be made by providing a homologous repair template and exploiting the homology directed repair pathway.
    B. Mutated Cas9 makes a site specific single-strand nick. Two sgRNA can be used to introduce a staggered double-stranded break which can then undergo homology directed repair.
    C. Nuclease-deficient Cas9 can be fused with various effector domains allowing specific localization. For example, transcriptional activators, repressors, and fluorescent proteins.

Targeting Efficiency and Off-target Mutations

Targeting efficiency, or the percentage of desired mutation achieved, is one of the most important parameters by which to assess a genome-editing tool. The targeting efficiency of Cas9 compares favorably with more established methods, such as TALENs or ZFNs (8). For example, in human cells, custom-designed ZFNs and TALENs could only achieve efficiencies ranging from 1% to 50% (29–31). In contrast, the Cas9 system has been reported to have efficiencies up to >70% in zebrafish (32) and plants (33), and ranging from 2–5% in induced pluripotent stem cells (34). In addition, Zhou and colleagues were able to improve genome targeting up to 78% in one-cell mouse embryos, and achieved effective germline transmission through the use of dual sgRNAs to simultaneously target an individual gene (35).

A widely used method to identify mutations is the T7 Endonuclease I mutation detection assay (36, 37) (Figure 3). This assay detects heteroduplex DNA that results from the annealing of a DNA strand, including desired mutations, with a wildtype DNA strand (37).

Figure 3. T7 Endonuclease I Targeting Efficiency Assay

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Genomic DNA is amplified with primers bracketing the modified locus. PCR products are then denatured and re-annealed yielding 3 possible structures. Duplexes containing a mismatch are digested by T7 Endonuclease I. The DNA is then electrophoretically separated and fragment analysis is used to calculate targeting efficiency.

Another important parameter is the incidence of off-target mutations. Such mutations are likely to appear in sites that have differences of only a few nucleotides compared to the original sequence, as long as they are adjacent to a PAM sequence. This occurs as Cas9 can tolerate up to 5 base mismatches within the protospacer region (36) or a single base difference in the PAM sequence (38). Off-target mutations are generally more difficult to detect, requiring whole-genome sequencing to rule them out completely.

Recent improvements to the CRISPR system for reducing off-target mutations have been made through the use of truncated gRNA (truncated within the crRNA-derived sequence) or by adding two extra guanine (G) nucleotides to the 5´ end (28, 37). Another way researchers have attempted to minimize off-target effects is with the use of “paired nickases” (20). This strategy uses D10A Cas9 and two sgRNAs complementary to the adjacent area on opposite strands of the target site (Figure 2B). While this induces DSBs in the target DNA, it is expected to create only single nicks in off-target locations and, therefore, result in minimal off-target mutations.

By leveraging computation to reduce off-target mutations, several groups have developed webbased tools to facilitate the identification of potential CRISPR target sites and assess their potential for off-target cleavage. Examples include the CRISPR Design Tool (38) and the ZiFiT Targeter, Version 4.2 (39, 40).

Applications as a Genome-editing and Genome Targeting Tool

Following its initial demonstration in 2012 (9), the CRISPR/Cas9 system has been widely adopted. This has already been successfully used to target important genes in many cell lines and organisms, including human (34), bacteria (41), zebrafish (32), C. elegans (42), plants (34), Xenopus tropicalis (43), yeast (44), Drosophila (45), monkeys (46), rabbits (47), pigs (42), rats (48) and mice (49). Several groups have now taken advantage of this method to introduce single point mutations (deletions or insertions) in a particular target gene, via a single gRNA (14, 21, 29). Using a pair of gRNA-directed Cas9 nucleases instead, it is also possible to induce large deletions or genomic rearrangements, such as inversions or translocations (50). A recent exciting development is the use of the dCas9 version of the CRISPR/Cas9 system to target protein domains for transcriptional regulation (26, 51, 52), epigenetic modification (25), and microscopic visualization of specific genome loci (27).

The CRISPR/Cas9 system requires only the redesign of the crRNA to change target specificity. This contrasts with other genome editing tools, including zinc finger and TALENs, where redesign of the protein-DNA interface is required. Furthermore, CRISPR/Cas9 enables rapid genome-wide interrogation of gene function by generating large gRNA libraries (51, 53) for genomic screening.

The Future of CRISPR/Cas9

The rapid progress in developing Cas9 into a set of tools for cell and molecular biology research has been remarkable, likely due to the simplicity, high efficiency and versatility of the system. Of the designer nuclease systems currently available for precision genome engineering, the CRISPR/Cas system is by far the most user friendly. It is now also clear that Cas9’s potential reaches beyond DNA cleavage, and its usefulness for genome locus-specific recruitment of proteins will likely only be limited by our imagination.

 

Scientists urge caution in using new CRISPR technology to treat human genetic disease

By Robert Sanders, Media relations | MARCH 19, 2015
http://news.berkeley.edu/2015/03/19/scientists-urge-caution-in-using-new-crispr-technology-to-treat-human-genetic-disease/

http://news.berkeley.edu/wp-content/uploads/2015/03/crispr350.jpg

The bacterial enzyme Cas9 is the engine of RNA-programmed genome engineering in human cells. (Graphic by Jennifer Doudna/UC Berkeley)

A group of 18 scientists and ethicists today warned that a revolutionary new tool to cut and splice DNA should be used cautiously when attempting to fix human genetic disease, and strongly discouraged any attempts at making changes to the human genome that could be passed on to offspring.

Among the authors of this warning is Jennifer Doudna, the co-inventor of the technology, called CRISPR-Cas9, which is driving a new interest in gene therapy, or “genome engineering.” She and colleagues co-authored a perspective piece that appears in the March 20 issue of Science, based on discussions at a meeting that took place in Napa on Jan. 24. The same issue of Science features a collection of recent research papers, commentary and news articles on CRISPR and its implications.    …..

A prudent path forward for genomic engineering and germline gene modification

David Baltimore1,  Paul Berg2, …., Jennifer A. Doudna4,10,*, et al.
http://science.sciencemag.org/content/early/2015/03/18/science.aab1028.full
Science  19 Mar 2015.  http://dx.doi.org:/10.1126/science.aab1028

 

Correcting genetic defects

Scientists today are changing DNA sequences to correct genetic defects in animals as well as cultured tissues generated from stem cells, strategies that could eventually be used to treat human disease. The technology can also be used to engineer animals with genetic diseases mimicking human disease, which could lead to new insights into previously enigmatic disorders.

The CRISPR-Cas9 tool is still being refined to ensure that genetic changes are precisely targeted, Doudna said. Nevertheless, the authors met “… to initiate an informed discussion of the uses of genome engineering technology, and to identify proactively those areas where current action is essential to prepare for future developments. We recommend taking immediate steps toward ensuring that the application of genome engineering technology is performed safely and ethically.”

 

Amyloid CRISPR Plasmids and si/shRNA Gene Silencers

http://www.scbt.com/crispr/table-amyloid.html

Santa Cruz Biotechnology, Inc. offers a broad range of gene silencers in the form of siRNAs, shRNA Plasmids and shRNA Lentiviral Particles as well as CRISPR/Cas9 Knockout and CRISPR Double Nickase plasmids. Amyloid gene silencers are available as Amyloid siRNA, Amyloid shRNA Plasmid, Amyloid shRNA Lentiviral Particles and Amyloid CRISPR/Cas9 Knockout plasmids. Amyloid CRISPR/dCas9 Activation Plasmids and CRISPR Lenti Activation Systems for gene activation are also available. Gene silencers and activators are useful for gene studies in combination with antibodies used for protein detection.    Amyloid CRISPR Knockout, HDR and Nickase Knockout Plasmids

 

CRISPR-Cas9-Based Knockout of the Prion Protein and Its Effect on the Proteome


Mehrabian M, Brethour D, MacIsaac S, Kim JK, Gunawardana C.G, Wang H, et al.
PLoS ONE 2014; 9(12): e114594. http://dx.doi.org/10.1371/journal.pone.0114594

The molecular function of the cellular prion protein (PrPC) and the mechanism by which it may contribute to neurotoxicity in prion diseases and Alzheimer’s disease are only partially understood. Mouse neuroblastoma Neuro2a cells and, more recently, C2C12 myocytes and myotubes have emerged as popular models for investigating the cellular biology of PrP. Mouse epithelial NMuMG cells might become attractive models for studying the possible involvement of PrP in a morphogenetic program underlying epithelial-to-mesenchymal transitions. Here we describe the generation of PrP knockout clones from these cell lines using CRISPR-Cas9 knockout technology. More specifically, knockout clones were generated with two separate guide RNAs targeting recognition sites on opposite strands within the first hundred nucleotides of the Prnp coding sequence. Several PrP knockout clones were isolated and genomic insertions and deletions near the CRISPR-target sites were characterized. Subsequently, deep quantitative global proteome analyses that recorded the relative abundance of>3000 proteins (data deposited to ProteomeXchange Consortium) were undertaken to begin to characterize the molecular consequences of PrP deficiency. The levels of ∼120 proteins were shown to reproducibly correlate with the presence or absence of PrP, with most of these proteins belonging to extracellular components, cell junctions or the cytoskeleton.

http://journals.plos.org/plosone/article/figure/image?size=inline&id=info:doi/10.1371/journal.pone.0114594.g001

http://journals.plos.org/plosone/article/figure/image?size=inline&id=info:doi/10.1371/journal.pone.0114594.g003

 

Development and Applications of CRISPR-Cas9 for Genome Engineering

Patrick D. Hsu,1,2,3 Eric S. Lander,1 and Feng Zhang1,2,*
Cell. 2014 Jun 5; 157(6): 1262–1278.   doi:  10.1016/j.cell.2014.05.010

Recent advances in genome engineering technologies based on the CRISPR-associated RNA-guided endonuclease Cas9 are enabling the systematic interrogation of mammalian genome function. Analogous to the search function in modern word processors, Cas9 can be guided to specific locations within complex genomes by a short RNA search string. Using this system, DNA sequences within the endogenous genome and their functional outputs are now easily edited or modulated in virtually any organism of choice. Cas9-mediated genetic perturbation is simple and scalable, empowering researchers to elucidate the functional organization of the genome at the systems level and establish causal linkages between genetic variations and biological phenotypes. In this Review, we describe the development and applications of Cas9 for a variety of research or translational applications while highlighting challenges as well as future directions. Derived from a remarkable microbial defense system, Cas9 is driving innovative applications from basic biology to biotechnology and medicine.

The development of recombinant DNA technology in the 1970s marked the beginning of a new era for biology. For the first time, molecular biologists gained the ability to manipulate DNA molecules, making it possible to study genes and harness them to develop novel medicine and biotechnology. Recent advances in genome engineering technologies are sparking a new revolution in biological research. Rather than studying DNA taken out of the context of the genome, researchers can now directly edit or modulate the function of DNA sequences in their endogenous context in virtually any organism of choice, enabling them to elucidate the functional organization of the genome at the systems level, as well as identify causal genetic variations.

Broadly speaking, genome engineering refers to the process of making targeted modifications to the genome, its contexts (e.g., epigenetic marks), or its outputs (e.g., transcripts). The ability to do so easily and efficiently in eukaryotic and especially mammalian cells holds immense promise to transform basic science, biotechnology, and medicine (Figure 1).

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4343198/bin/nihms659174f1.jpg

For life sciences research, technologies that can delete, insert, and modify the DNA sequences of cells or organisms enable dissecting the function of specific genes and regulatory elements. Multiplexed editing could further allow the interrogation of gene or protein networks at a larger scale. Similarly, manipulating transcriptional regulation or chromatin states at particular loci can reveal how genetic material is organized and utilized within a cell, illuminating relationships between the architecture of the genome and its functions. In biotechnology, precise manipulation of genetic building blocks and regulatory machinery also facilitates the reverse engineering or reconstruction of useful biological systems, for example, by enhancing biofuel production pathways in industrially relevant organisms or by creating infection-resistant crops. Additionally, genome engineering is stimulating a new generation of drug development processes and medical therapeutics. Perturbation of multiple genes simultaneously could model the additive effects that underlie complex polygenic disorders, leading to new drug targets, while genome editing could directly correct harmful mutations in the context of human gene therapy (Tebas et al., 2014).

Eukaryotic genomes contain billions of DNA bases and are difficult to manipulate. One of the breakthroughs in genome manipulation has been the development of gene targeting by homologous recombination (HR), which integrates exogenous repair templates that contain sequence homology to the donor site (Figure 2A) (Capecchi, 1989). HR-mediated targeting has facilitated the generation of knockin and knockout animal models via manipulation of germline competent stem cells, dramatically advancing many areas of biological research. However, although HR-mediated gene targeting produces highly precise alterations, the desired recombination events occur extremely infrequently (1 in 106–109 cells) (Capecchi, 1989), presenting enormous challenges for large-scale applications of gene-targeting experiments.

Genome Editing Technologies Exploit Endogenous DNA Repair Machinery

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4343198/bin/nihms659174f2.gif

To overcome these challenges, a series of programmable nuclease-based genome editing technologies have been developed in recent years, enabling targeted and efficient modification of a variety of eukaryotic and particularly mammalian species. Of the current generation of genome editing technologies, the most rapidly developing is the class of RNA-guided endonucleases known as Cas9 from the microbial adaptive immune system CRISPR (clustered regularly interspaced short palindromic repeats), which can be easily targeted to virtually any genomic location of choice by a short RNA guide. Here, we review the development and applications of the CRISPR-associated endonuclease Cas9 as a platform technology for achieving targeted perturbation of endogenous genomic elements and also discuss challenges and future avenues for innovation.   ……

Figure 4   Natural Mechanisms of Microbial CRISPR Systems in Adaptive Immunity

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4343198/bin/nihms659174f4.gif

……  A key turning point came in 2005, when systematic analysis of the spacer sequences separating the individual direct repeats suggested their extrachromosomal and phage-associated origins (Mojica et al., 2005Pourcel et al., 2005Bolotin et al., 2005). This insight was tremendously exciting, especially given previous studies showing that CRISPR loci are transcribed (Tang et al., 2002) and that viruses are unable to infect archaeal cells carrying spacers corresponding to their own genomes (Mojica et al., 2005). Together, these findings led to the speculation that CRISPR arrays serve as an immune memory and defense mechanism, and individual spacers facilitate defense against bacteriophage infection by exploiting Watson-Crick base-pairing between nucleic acids (Mojica et al., 2005Pourcel et al., 2005). Despite these compelling realizations that CRISPR loci might be involved in microbial immunity, the specific mechanism of how the spacers act to mediate viral defense remained a challenging puzzle. Several hypotheses were raised, including thoughts that CRISPR spacers act as small RNA guides to degrade viral transcripts in a RNAi-like mechanism (Makarova et al., 2006) or that CRISPR spacers direct Cas enzymes to cleave viral DNA at spacer-matching regions (Bolotin et al., 2005).   …..

As the pace of CRISPR research accelerated, researchers quickly unraveled many details of each type of CRISPR system (Figure 4). Building on an earlier speculation that protospacer adjacent motifs (PAMs) may direct the type II Cas9 nuclease to cleave DNA (Bolotin et al., 2005), Moineau and colleagues highlighted the importance of PAM sequences by demonstrating that PAM mutations in phage genomes circumvented CRISPR interference (Deveau et al., 2008). Additionally, for types I and II, the lack of PAM within the direct repeat sequence within the CRISPR array prevents self-targeting by the CRISPR system. In type III systems, however, mismatches between the 5′ end of the crRNA and the DNA target are required for plasmid interference (Marraffini and Sontheimer, 2010).  …..

In 2013, a pair of studies simultaneously showed how to successfully engineer type II CRISPR systems from Streptococcus thermophilus (Cong et al., 2013) andStreptococcus pyogenes (Cong et al., 2013Mali et al., 2013a) to accomplish genome editing in mammalian cells. Heterologous expression of mature crRNA-tracrRNA hybrids (Cong et al., 2013) as well as sgRNAs (Cong et al., 2013Mali et al., 2013a) directs Cas9 cleavage within the mammalian cellular genome to stimulate NHEJ or HDR-mediated genome editing. Multiple guide RNAs can also be used to target several genes at once. Since these initial studies, Cas9 has been used by thousands of laboratories for genome editing applications in a variety of experimental model systems (Sander and Joung, 2014). ……

The majority of CRISPR-based technology development has focused on the signature Cas9 nuclease from type II CRISPR systems. However, there remains a wide diversity of CRISPR types and functions. Cas RAMP module (Cmr) proteins identified in Pyrococcus furiosus and Sulfolobus solfataricus (Hale et al., 2012) constitute an RNA-targeting CRISPR immune system, forming a complex guided by small CRISPR RNAs that target and cleave complementary RNA instead of DNA. Cmr protein homologs can be found throughout bacteria and archaea, typically relying on a 5 site tag sequence on the target-matching crRNA for Cmr-directed cleavage.

Unlike RNAi, which is targeted largely by a 6 nt seed region and to a lesser extent 13 other bases, Cmr crRNAs contain 30–40 nt of target complementarity. Cmr-CRISPR technologies for RNA targeting are thus a promising target for orthogonal engineering and minimal off-target modification. Although the modularity of Cmr systems for RNA-targeting in mammalian cells remains to be investigated, Cmr complexes native to P. furiosus have already been engineered to target novel RNA substrates (Hale et al., 20092012).   ……

Although Cas9 has already been widely used as a research tool, a particularly exciting future direction is the development of Cas9 as a therapeutic technology for treating genetic disorders. For a monogenic recessive disorder due to loss-of-function mutations (such as cystic fibrosis, sickle-cell anemia, or Duchenne muscular dystrophy), Cas9 may be used to correct the causative mutation. This has many advantages over traditional methods of gene augmentation that deliver functional genetic copies via viral vector-mediated overexpression—particularly that the newly functional gene is expressed in its natural context. For dominant-negative disorders in which the affected gene is haplosufficient (such as transthyretin-related hereditary amyloidosis or dominant forms of retinitis pigmentosum), it may also be possible to use NHEJ to inactivate the mutated allele to achieve therapeutic benefit. For allele-specific targeting, one could design guide RNAs capable of distinguishing between single-nucleotide polymorphism (SNP) variations in the target gene, such as when the SNP falls within the PAM sequence.

 

 

CRISPR/Cas9: a powerful genetic engineering tool for establishing large animal models of neurodegenerative diseases

Zhuchi Tu, Weili Yang, Sen Yan, Xiangyu Guo and Xiao-Jiang Li

Molecular Neurodegeneration 2015; 10:35  http://dx.doi.org:/10.1186/s13024-015-0031-x

Animal models are extremely valuable to help us understand the pathogenesis of neurodegenerative disorders and to find treatments for them. Since large animals are more like humans than rodents, they make good models to identify the important pathological events that may be seen in humans but not in small animals; large animals are also very important for validating effective treatments or confirming therapeutic targets. Due to the lack of embryonic stem cell lines from large animals, it has been difficult to use traditional gene targeting technology to establish large animal models of neurodegenerative diseases. Recently, CRISPR/Cas9 was used successfully to genetically modify genomes in various species. Here we discuss the use of CRISPR/Cas9 technology to establish large animal models that can more faithfully mimic human neurodegenerative diseases.

Neurodegenerative diseases — Alzheimer’s disease(AD),Parkinson’s disease(PD), amyotrophic lateral sclerosis (ALS), Huntington’s disease (HD), and frontotemporal dementia (FTD) — are characterized by age-dependent and selective neurodegeneration. As the life expectancy of humans lengthens, there is a greater prevalence of these neurodegenerative diseases; however, the pathogenesis of most of these neurodegenerative diseases remain unclear, and we lack effective treatments for these important brain disorders.

CRISPR/Cas9,  Non-human primates,  Neurodegenerative diseases,  Animal model

There are a number of excellent reviews covering different types of neurodegenerative diseases and their genetic mouse models [812]. Investigations of different mouse models of neurodegenerative diseases have revealed a common pathology shared by these diseases. First, the development of neuropathology and neurological symptoms in genetic mouse models of neurodegenerative diseases is age dependent and progressive. Second, all the mouse models show an accumulation of misfolded or aggregated proteins resulting from the expression of mutant genes. Third, despite the widespread expression of mutant proteins throughout the body and brain, neuronal function appears to be selectively or preferentially affected. All these facts indicate that mouse models of neurodegenerative diseases recapitulate important pathologic features also seen in patients with neurodegenerative diseases.

However, it seems that mouse models can not recapitulate the full range of neuropathology seen in patients with neurodegenerative diseases. Overt neurodegeneration, which is the most important pathological feature in patient brains, is absent in genetic rodent models of AD, PD, and HD. Many rodent models that express transgenic mutant proteins under the control of different promoters do not replicate overt neurodegeneration, which is likely due to their short life spans and the different aging processes of small animals. Also important are the remarkable differences in brain development between rodents and primates. For example, the mouse brain takes 21 days to fully develop, whereas the formation of primate brains requires more than 150 days [13]. The rapid development of the brain in rodents may render neuronal cells resistant to misfolded protein-mediated neurodegeneration. Another difficulty in using rodent models is how to analyze cognitive and emotional abnormalities, which are the early symptoms of most neurodegenerative diseases in humans. Differences in neuronal circuitry, anatomy, and physiology between rodent and primate brains may also account for the behavioral differences between rodent and primate models.

 

Mitochondrial dynamics–fusion, fission, movement, and mitophagy–in neurodegenerative diseases

Hsiuchen Chen and David C. Chan
Human Molec Gen 2009; 18, Review Issue 2 R169–R176
http://dx.doi.org:/10.1093/hmg/ddp326

Neurons are metabolically active cells with high energy demands at locations distant from the cell body. As a result, these cells are particularly dependent on mitochondrial function, as reflected by the observation that diseases of mitochondrial dysfunction often have a neurodegenerative component. Recent discoveries have highlighted that neurons are reliant particularly on the dynamic properties of mitochondria. Mitochondria are dynamic organelles by several criteria. They engage in repeated cycles of fusion and fission, which serve to intermix the lipids and contents of a population of mitochondria. In addition, mitochondria are actively recruited to subcellular sites, such as the axonal and dendritic processes of neurons. Finally, the quality of a mitochondrial population is maintained through mitophagy, a form of autophagy in which defective mitochondria are selectively degraded. We review the general features of mitochondrial dynamics, incorporating recent findings on mitochondrial fusion, fission, transport and mitophagy. Defects in these key features are associated with neurodegenerative disease. Charcot-Marie-Tooth type 2A, a peripheral neuropathy, and dominant optic atrophy, an inherited optic neuropathy, result from a primary deficiency of mitochondrial fusion. Moreover, several major neurodegenerative diseases—including Parkinson’s, Alzheimer’s and Huntington’s disease—involve disruption of mitochondrial dynamics. Remarkably, in several disease models, the manipulation of mitochondrial fusion or fission can partially rescue disease phenotypes. We review how mitochondrial dynamics is altered in these neurodegenerative diseases and discuss the reciprocal interactions between mitochondrial fusion, fission, transport and mitophagy.

 

Applications of CRISPR–Cas systems in Neuroscience

Matthias Heidenreich  & Feng Zhang
Nature Rev Neurosci 2016; 17:36–44   http://dx.doi.org:/10.1038/nrn.2015.2

Genome-editing tools, and in particular those based on CRISPR–Cas (clustered regularly interspaced short palindromic repeat (CRISPR)–CRISPR-associated protein) systems, are accelerating the pace of biological research and enabling targeted genetic interrogation in almost any organism and cell type. These tools have opened the door to the development of new model systems for studying the complexity of the nervous system, including animal models and stem cell-derived in vitro models. Precise and efficient gene editing using CRISPR–Cas systems has the potential to advance both basic and translational neuroscience research.
Cellular neuroscience
, DNA recombination, Genetic engineering, Molecular neuroscience

Figure 3: In vitro applications of Cas9 in human iPSCs.close

http://www.nature.com/nrn/journal/v17/n1/carousel/nrn.2015.2-f3.jpg

a | Evaluation of disease candidate genes from large-population genome-wide association studies (GWASs). Human primary cells, such as neurons, are not easily available and are difficult to expand in culture. By contrast, induced pluripo…

  1. Genome-editing Technologies for Gene and Cell Therapy

Molecular Therapy 12 Jan 2016

  1. Systematic quantification of HDR and NHEJ reveals effects of locus, nuclease, and cell type on genome-editing

Scientific Reports 31 Mar 2016

  1. Controlled delivery of β-globin-targeting TALENs and CRISPR/Cas9 into mammalian cells for genome editing using microinjection

Scientific Reports 12 Nov 2015

 

Alzheimer’s Disease: Medicine’s Greatest Challenge in the 21st Century

https://www.physicsforums.com/insights/can-gene-editing-eliminate-alzheimers-disease/

The development of the CRISPR/Cas9 system has made gene editing a relatively simple task.  While CRISPR and other gene editing technologies stand to revolutionize biomedical research and offers many promising therapeutic avenues (such as in the treatment of HIV), a great deal of debate exists over whether CRISPR should be used to modify human embryos. As I discussed in my previous Insight article, we lack enough fundamental biological knowledge to enhance many traits like height or intelligence, so we are not near a future with genetically-enhanced super babies. However, scientists have identified a few rare genetic variants that protect against disease.  One such protective variant is a mutation in the APP gene that protects against Alzheimer’s disease and cognitive decline in old age. If we can perfect gene editing technologies, is this mutation one that we should be regularly introducing into embryos? In this article, I explore the potential for using gene editing as a way to prevent Alzheimer’s disease in future generations. Alzheimer’s Disease: Medicine’s Greatest Challenge in the 21st Century Can gene editing be the missing piece in the battle against Alzheimer’s? (Source: bostonbiotech.org) I chose to assess the benefit of germline gene editing in the context of Alzheimer’s disease because this disease is one of the biggest challenges medicine faces in the 21st century. Alzheimer’s disease is a chronic neurodegenerative disease responsible for the majority of the cases of dementia in the elderly. The disease symptoms begins with short term memory loss and causes more severe symptoms – problems with language, disorientation, mood swings, behavioral issues – as it progresses, eventually leading to the loss of bodily functions and death. Because of the dementia the disease causes, Alzheimer’s patients require a great deal of care, and the world spends ~1% of its total GDP on caring for those with Alzheimer’s and related disorders. Because the prevalence of the disease increases with age, the situation will worsen as life expectancies around the globe increase: worldwide cases of Alzheimer’s are expected to grow from 35 million today to over 115 million by 2050.

Despite much research, the exact causes of Alzheimer’s disease remains poorly understood. The disease seems to be related to the accumulation of plaques made of amyloid-β peptides that form on the outside of neurons, as well as the formation of tangles of the protein tau inside of neurons. Although many efforts have been made to target amyloid-β or the enzymes involved in its formation, we have so far been unsuccessful at finding any treatment that stops the disease or reverses its progress. Some researchers believe that most attempts at treating Alzheimer’s have failed because, by the time a patient shows symptoms, the disease has already progressed past the point of no return.

While research towards a cure continues, researchers have sought effective ways to prevent Alzheimer’s disease. Although some studies show that mental and physical exercise may lower ones risk of Alzheimer’s disease, approximately 60-80% of the risk for Alzheimer’s disease appears to be genetic. Thus, if we’re serious about prevention, we may have to act at the genetic level. And because the brain is difficult to access surgically for gene therapy in adults, this means using gene editing on embryos.

Reference https://www.physicsforums.com/insights/can-gene-editing-eliminate-alzheimers-disease/

 

Utilising CRISPR to Generate Predictive Disease Models: a Case Study in Neurodegenerative Disorders


Dr. Bhuvaneish.T. Selvaraj  – Scottish Centre for Regenerative Medicine

http://www.crisprsummit.com/utilising-crispr-to-generate-predictive-disease-models-a-case-study-in-neurodegenerative-disorders

  • Introducing the latest developments in predictive model generation
  • Discover how CRISPR is being used to develop disease models to study and treat neurodegenerative disorders
  • In depth Q&A session to answer your most pressing questions

 

Turning On Genes, Systematically, with CRISPR/Cas9

http://www.genengnews.com/gen-news-highlights/turning-on-genes-systematically-with-crispr-cas9/81250697/

 

Scientists based at MIT assert that they can reliably turn on any gene of their choosing in living cells. [Feng Zhang and Steve Dixon]  http://www.genengnews.com/media/images/GENHighlight/Dec12_2014_CRISPRCas9GeneActivationSystem7838101231.jpg

With the latest CRISPR/Cas9 advance, the exhortation “turn on, tune in, drop out” comes to mind. The CRISPR/Cas9 gene-editing system was already a well-known means of “tuning in” (inserting new genes) and “dropping out” (knocking out genes). But when it came to “turning on” genes, CRISPR/Cas9 had little potency. That is, it had demonstrated only limited success as a way to activate specific genes.

A new CRISPR/Cas9 approach, however, appears capable of activating genes more effectively than older approaches. The new approach may allow scientists to more easily determine the function of individual genes, according to Feng Zhang, Ph.D., a researcher at MIT and the Broad Institute. Dr. Zhang and colleagues report that the new approach permits multiplexed gene activation and rapid, large-scale studies of gene function.

The new technique was introduced in the December 10 online edition of Nature, in an article entitled, “Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex.” The article describes how Dr. Zhang, along with the University of Tokyo’s Osamu Nureki, Ph.D., and Hiroshi Nishimasu, Ph.D., overhauled the CRISPR/Cas9 system. The research team based their work on their analysis (published earlier this year) of the structure formed when Cas9 binds to the guide RNA and its target DNA. Specifically, the team used the structure’s 3D shape to rationally improve the system.

In previous efforts to revamp CRISPR/Cas9 for gene activation purposes, scientists had tried to attach the activation domains to either end of the Cas9 protein, with limited success. From their structural studies, the MIT team realized that two small loops of the RNA guide poke out from the Cas9 complex and could be better points of attachment because they allow the activation domains to have more flexibility in recruiting transcription machinery.

Using their revamped system, the researchers activated about a dozen genes that had proven difficult or impossible to turn on using the previous generation of Cas9 activators. Each gene showed at least a twofold boost in transcription, and for many genes, the researchers found multiple orders of magnitude increase in activation.

After investigating single-guide RNA targeting rules for effective transcriptional activation, demonstrating multiplexed activation of 10 genes simultaneously, and upregulating long intergenic noncoding RNA transcripts, the research team decided to undertake a large-scale screen. This screen was designed to identify genes that confer resistance to a melanoma drug called PLX-4720.

“We … synthesized a library consisting of 70,290 guides targeting all human RefSeq coding isoforms to screen for genes that, upon activation, confer resistance to a BRAF inhibitor,” wrote the authors of the Nature paper. “The top hits included genes previously shown to be able to confer resistance, and novel candidates were validated using individual [single-guide RNA] and complementary DNA overexpression.”

A gene signature based on the top screening hits, the authors added, correlated with a gene expression signature of BRAF inhibitor resistance in cell lines and patient-derived samples. It was also suggested that large-scale screens such as the one demonstrated in the current study could help researchers discover new cancer drugs that prevent tumors from becoming resistant.

More at –  http://www.genengnews.com/gen-news-highlights/turning-on-genes-systematically-with-crispr-cas9/81250697/

 

Susceptibility and modifier genes in Portuguese transthyretin V30M amyloid polyneuropathy: complexity in a single-gene disease
Miguel L. Soares1,2, Teresa Coelho3,6, Alda Sousa4,5, …, Maria Joa˜o Saraiva2,5 and Joel N. Buxbaum1
Human Molec Gen 2005; 14(4): 543–553   http://dx.doi.org:/10.1093/hmg/ddi051
https://www.researchgate.net/profile/Isabel_Conceicao/publication/8081351_Susceptibility_and_modifier_genes_in_Portuguese_transthyretin_V30M_amyloid_polyneuropathy_complexity_in_a_single-gene_disease/links/53e123d70cf2235f352733b3.pdf

Familial amyloid polyneuropathy type I is an autosomal dominant disorder caused by mutations in the transthyretin (TTR ) gene; however, carriers of the same mutation exhibit variability in penetrance and clinical expression. We analyzed alleles of candidate genes encoding non-fibrillar components of TTR amyloid deposits and a molecule metabolically interacting with TTR [retinol-binding protein (RBP)], for possible associations with age of disease onset and/or susceptibility in a Portuguese population sample with the TTR V30M mutation and unrelated controls. We show that the V30M carriers represent a distinct subset of the Portuguese population. Estimates of genetic distance indicated that the controls and the classical onset group were furthest apart, whereas the late-onset group appeared to differ from both. Importantly, the data also indicate that genetic interactions among the multiple loci evaluated, rather than single-locus effects, are more likely to determine differences in the age of disease onset. Multifactor dimensionality reduction indicated that the best genetic model for classical onset group versus controls involved the APCS gene, whereas for late-onset cases, one APCS variant (APCSv1) and two RBP variants (RBPv1 and RBPv2) are involved. Thus, although the TTR V30M mutation is required for the disease in Portuguese patients, different genetic factors may govern the age of onset, as well as the occurrence of anticipation.

Autosomal dominant disorders may vary in expression even within a given kindred. The basis of this variability is uncertain and can be attributed to epigenetic factors, environment or epistasis. We have studied familial amyloid polyneuropathy (FAP), an autosomal dominant disorder characterized by peripheral sensorimotor and autonomic neuropathy. It exhibits variation in cardiac, renal, gastrointestinal and ocular involvement, as well as age of onset. Over 80 missense mutations in the transthyretin gene (TTR ) result in autosomal dominant disease http://www.ibmc.up.pt/~mjsaraiv/ttrmut.html). The presence of deposits consisting entirely of wild-type TTR molecules in the hearts of 10– 25% of individuals over age 80 reveals its inherent in vivo amyloidogenic potential (1).

FAP was initially described in Portuguese (2) where, until recently, the TTR V30M has been the only pathogenic mutation associated with the disease (3,4). Later reports identified the same mutation in Swedish and Japanese families (5,6). The disorder has since been recognized in other European countries and in North American kindreds in association with V30M, as well as other mutations (7).

TTR V30M produces disease in only 5–10% of Swedish carriers of the allele (8), a much lower degree of penetrance than that seen in Portuguese (80%) (9) or in Japanese with the same mutation. The actual penetrance in Japanese carriers has not been formally established, but appears to resemble that seen in Portuguese. Portuguese and Japanese carriers show considerable variation in the age of clinical onset (10,11). In both populations, the first symptoms had originally been described as typically occurring before age 40 (so-called ‘classical’ or early-onset); however, in recent years, more individuals developing symptoms late in life have been identified (11,12). Hence, present data indicate that the distribution of the age of onset in Portuguese is continuous, but asymmetric with a mean around age 35 and a long tail into the older age group (Fig. 1) (9,13). Further, DNA testing in Portugal has identified asymptomatic carriers over age 70 belonging to a subset of very late-onset kindreds in whose descendants genetic anticipation is frequent. The molecular basis of anticipation in FAP, which is not mediated by trinucleotide repeat expansions in the TTR or any other gene (14), remains elusive.

Variation in penetrance, age of onset and clinical features are hallmarks of many autosomal dominant disorders including the human TTR amyloidoses (7). Some of these clearly reflect specific biological effects of a particular mutation or a class of mutants. However, when such phenotypic variability is seen with a single mutation in the gene encoding the same protein, it suggests an effect of modifying genetic loci and/or environmental factors contributing differentially to the course of disease. We have chosen to examine age of onset as an example of a discrete phenotypic variation in the presence of the particular autosomal dominant disease-associated mutation TTR V30M. Although the role of environmental factors cannot be excluded, the existence of modifier genes involved in TTR amyloidogenesis is an attractive hypothesis to explain the phenotypic variability in FAP. ….

ATTR (TTR amyloid), like all amyloid deposits, contains several molecular components, in addition to the quantitatively dominant fibril-forming amyloid protein, including heparan sulfate proteoglycan 2 (HSPG2 or perlecan), SAP, a plasma glycoprotein of the pentraxin family (encoded by the APCS gene) that undergoes specific calcium-dependent binding to all types of amyloid fibrils, and apolipoprotein E (ApoE), also found in all amyloid deposits (15). The ApoE4 isoform is associated with an increased frequency and earlier onset of Alzheimer’s disease (Ab), the most common form of brain amyloid, whereas the ApoE2 isoform appears to be protective (16). ApoE variants could exert a similar modulatory effect in the onset of FAP, although early studies on a limited number of patients suggested this was not the case (17).

In at least one instance of senile systemic amyloidosis, small amounts of AA-related material were found in TTR deposits (18). These could reflect either a passive co-aggregation or a contributory involvement of protein AA, encoded by the serum amyloid A (SAA ) genes and the main component of secondary (reactive) amyloid fibrils, in the formation of ATTR.

Retinol-binding protein (RBP), the serum carrier of vitamin A, circulates in plasma bound to TTR. Vitamin A-loaded RBP and L-thyroxine, the two natural ligands of TTR, can act alone or synergistically to inhibit the rate and extent of TTR fibrillogenesis in vitro, suggesting that RBP may influence the course of FAP pathology in vivo (19). We have analyzed coding and non-coding sequence polymorphisms in the RBP4 (serum RBP, 10q24), HSPG2 (1p36.1), APCS (1q22), APOE (19q13.2), SAA1 and SAA2 (11p15.1) genes with the goal of identifying chromosomes carrying common and functionally significant variants. At the time these studies were performed, the full human genome sequence was not completed and systematic singlenucleotide polymorphism (SNP) analyses were not available for any of the suspected candidate genes. We identified new SNPs in APCS and RBP4 and utilized polymorphisms in SAA, HSPG2 and APOE that had already been characterized and shown to have potential pathophysiologic significance in other disorders (16,20–22). The genotyping data were analyzed for association with the presence of the V30M amyloidogenic allele (FAP patients versus controls) and with the age of onset (classical- versus late-onset patients). Multilocus analyses were also performed to examine the effects of simultaneous contributions of the six loci for determining the onset of the first symptoms.  …..

The potential for different underlying models for classical and late onset is supported by the MDR analysis, which produces two distinct models when comparing each class with the controls. One could view the two onset classes as unique diseases. If this is the case, then the failure to detect a single predictive genetic model is consistent with two related, but different, diseases. This is exactly what would be expected in such a case of genetic heterogeneity (28). Using this approach, a major gene effect can be viewed as a necessary, but not sufficient, condition to explain the course of the disease. Analyzing the cases but omitting from the analysis of phenotype the necessary allele, in this case TTR V30M, can then reveal a variety of important modifiers that are distinct between the phenotypes.

The significant comparisons obtained in our study cohort indicate that the combined effects mainly result from two and three-locus interactions involving all loci except SAA1 and SAA2 for susceptibility to disease. A considerable number of four-site combinations modulate the age of onset with SAA1 appearing in a majority of significant combinations in late-onset disease, perhaps indicating a greater role of the SAA variants in the age of onset of FAP.

The correlation between genotype and phenotype in socalled simple Mendelian disorders is often incomplete, as only a subset of all mutations can reliably predict specific phenotypes (34). This is because non-allelic genetic variations and/or environmental influences underlie these disorders whose phenotypes behave as complex traits. A few examples include the identification of the role of homozygozity for the SAA1.1 allele in conferring the genetic susceptibility to renal amyloidosis in FMF (20) and the association of an insertion/deletion polymorphism in the ACE gene with disease severity in familial hypertrophic cardiomyopathy (35). In these disorders, the phenotypes arise from mutations in MEFV and b-MHC, but are modulated by independently inherited genetic variation. In this report, we show that interactions among multiple genes, whose products are confirmed or putative constituents of ATTR deposits, or metabolically interact with TTR, modulate the onset of the first symptoms and predispose individuals to disease in the presence of the V30M mutation in TTR. The exact nature of the effects identified here requires further study with potential application in the development of genetic screening with prognostic value pertaining to the onset of disease in the TTR V30M carriers.

If the effects of additional single or interacting genes dictate the heterogeneity of phenotype, as reflected in variability of onset and clinical expression (with the same TTR mutation), the products encoded by alleles at such loci could contribute to the process of wild-type TTR deposition in elderly individuals without a mutation (senile systemic amyloidosis), a phenomenon not readily recognized as having a genetic basis because of the insensitivity of family history in the elderly.

 

Safety and Efficacy of RNAi Therapy for Transthyretin Amyloidosis

Coelho T, Adams D, Silva A, et al.
N Engl J Med 2013;369:819-29.    http://dx.doi.org:/10.1056/NEJMoa1208760

Transthyretin amyloidosis is caused by the deposition of hepatocyte-derived transthyretin amyloid in peripheral nerves and the heart. A therapeutic approach mediated by RNA interference (RNAi) could reduce the production of transthyretin.

Methods We identified a potent antitransthyretin small interfering RNA, which was encapsulated in two distinct first- and second-generation formulations of lipid nanoparticles, generating ALN-TTR01 and ALN-TTR02, respectively. Each formulation was studied in a single-dose, placebo-controlled phase 1 trial to assess safety and effect on transthyretin levels. We first evaluated ALN-TTR01 (at doses of 0.01 to 1.0 mg per kilogram of body weight) in 32 patients with transthyretin amyloidosis and then evaluated ALN-TTR02 (at doses of 0.01 to 0.5 mg per kilogram) in 17 healthy volunteers.

Results Rapid, dose-dependent, and durable lowering of transthyretin levels was observed in the two trials. At a dose of 1.0 mg per kilogram, ALN-TTR01 suppressed transthyretin, with a mean reduction at day 7 of 38%, as compared with placebo (P=0.01); levels of mutant and nonmutant forms of transthyretin were lowered to a similar extent. For ALN-TTR02, the mean reductions in transthyretin levels at doses of 0.15 to 0.3 mg per kilogram ranged from 82.3 to 86.8%, with reductions of 56.6 to 67.1% at 28 days (P<0.001 for all comparisons). These reductions were shown to be RNAi mediated. Mild-to-moderate infusion-related reactions occurred in 20.8% and 7.7% of participants receiving ALN-TTR01 and ALN-TTR02, respectively.

ALN-TTR01 and ALN-TTR02 suppressed the production of both mutant and nonmutant forms of transthyretin, establishing proof of concept for RNAi therapy targeting messenger RNA transcribed from a disease-causing gene.

 

Alnylam May Seek Approval for TTR Amyloidosis Rx in 2017 as Other Programs Advance


https://www.genomeweb.com/rnai/alnylam-may-seek-approval-ttr-amyloidosis-rx-2017-other-programs-advance

Officials from Alnylam Pharmaceuticals last week provided updates on the two drug candidates from the company’s flagship transthyretin-mediated amyloidosis program, stating that the intravenously delivered agent patisiran is proceeding toward a possible market approval in three years, while a subcutaneously administered version called ALN-TTRsc is poised to enter Phase III testing before the end of the year.

Meanwhile, Alnylam is set to advance a handful of preclinical therapies into human studies in short order, including ones for complement-mediated diseases, hypercholesterolemia, and porphyria.

The officials made their comments during a conference call held to discuss Alnylam’s second-quarter financial results.

ATTR is caused by a mutation in the TTR gene, which normally produces a protein that acts as a carrier for retinol binding protein and is characterized by the accumulation of amyloid deposits in various tissues. Alnylam’s drugs are designed to silence both the mutant and wild-type forms of TTR.

Patisiran, which is delivered using lipid nanoparticles developed by Tekmira Pharmaceuticals, is currently in a Phase III study in patients with a form of ATTR called familial amyloid polyneuropathy (FAP) affecting the peripheral nervous system. Running at over 20 sites in nine countries, that study is set to enroll up to 200 patients and compare treatment to placebo based on improvements in neuropathy symptoms.

According to Alnylam Chief Medical Officer Akshay Vaishnaw, Alnylam expects to have final data from the study in two to three years, which would put patisiran on track for a new drug application filing in 2017.

Meanwhile, ALN-TTRsc, which is under development for a version of ATTR that affects cardiac tissue called familial amyloidotic cardiomyopathy (FAC) and uses Alnylam’s proprietary GalNAc conjugate delivery technology, is set to enter Phase III by year-end as Alnylam holds “active discussions” with US and European regulators on the design of that study, CEO John Maraganore noted during the call.

In the interim, Alnylam continues to enroll patients in a pilot Phase II study of ALN-TTRsc, which is designed to test the drug’s efficacy for FAC or senile systemic amyloidosis (SSA), a condition caused by the idiopathic accumulation of wild-type TTR protein in the heart.

Based on “encouraging” data thus far, Vaishnaw said that Alnylam has upped the expected enrollment in this study to 25 patients from 15. Available data from the trial is slated for release in November, he noted, stressing that “any clinical endpoint result needs to be considered exploratory given the small sample size and the very limited duration of treatment of only six weeks” in the trial.

Vaishnaw added that an open-label extension (OLE) study for patients in the ALN-TTRsc study will kick off in the coming weeks, allowing the company to gather long-term dosing tolerability and clinical activity data on the drug.

Enrollment in an OLE study of patisiran has been completed with 27 patients, he said, and, “as of today, with up to nine months of therapy … there have been no study drug discontinuations.” Clinical endpoint data from approximately 20 patients in this study will be presented at the American Neurological Association meeting in October.

As part of its ATTR efforts, Alnylam has also been conducting natural history of disease studies in both FAP and FAC patients. Data from the 283-patient FAP study was presented earlier this year and showed a rapid progression in neuropathy impairment scores and a high correlation of this measurement with disease severity.

During last week’s conference call, Vaishnaw said that clinical endpoint and biomarker data on about 400 patients with either FAC or SSA have already been collected in a nature history study on cardiac ATTR. Maraganore said that these findings would likely be released sometime next year.

Alnylam Presents New Phase II, Preclinical Data from TTR Amyloidosis Programs
https://www.genomeweb.com/rnai/alnylam-presents-new-phase-ii-preclinical-data-ttr-amyloidosis-programs

 

Amyloid disease drug approved

Nature Biotechnology 2012; (3http://dx.doi.org:/10.1038/nbt0212-121b

The first medication for a rare and often fatal protein misfolding disorder has been approved in Europe. On November 16, the E gave a green light to Pfizer’s Vyndaqel (tafamidis) for treating transthyretin amyloidosis in adult patients with stage 1 polyneuropathy symptoms. [Jeffery Kelly, La Jolla]

 

Safety and Efficacy of RNAi Therapy for Transthyretin …

http://www.nejm.org/…/NEJMoa1208760?&#8230;

The New England Journal of Medicine

Aug 29, 2013 – Transthyretin amyloidosis is caused by the deposition of hepatocyte-derived transthyretin amyloid in peripheral nerves and the heart.

 

Alnylam’s RNAi therapy targets amyloid disease

Ken Garber
Nature Biotechnology 2015; 33(577)    http://dx.doi.org:/10.1038/nbt0615-577a

RNA interference’s silencing of target genes could result in potent therapeutics.

http://www.nature.com/nbt/journal/v33/n6/images/nbt0615-577a-I1.jpg

The most clinically advanced RNA interference (RNAi) therapeutic achieved a milestone in April when Alnylam Pharmaceuticals in Cambridge, Massachusetts, reported positive results for patisiran, a small interfering RNA (siRNA) oligonucleotide targeting transthyretin for treating familial amyloidotic polyneuropathy (FAP).  …

  1. Analysis of 589,306 genomes identifies individuals resilient to severe Mendelian childhood diseases

Nature Biotechnology 11 April 2016

  1. CRISPR-Cas systems for editing, regulating and targeting genomes

Nature Biotechnology 02 March 2014

  1. Near-optimal probabilistic RNA-seq quantification

Nature Biotechnology 04 April 2016

 

Translational Neuroscience: Toward New Therapies

https://books.google.com/books?isbn=0262029863

Karoly Nikolich, ‎Steven E. Hyman – 2015 – ‎Medical

Tafamidis for Transthyretin Familial Amyloid Polyneuropathy: A Randomized, Controlled Trial. … Multiplex Genome Engineering Using CRISPR/Cas Systems.

 

Is CRISPR a Solution to Familial Amyloid Polyneuropathy?

Author and Curator: Larry H. Bernstein, MD, FCAP

Originally published as

https://pharmaceuticalintelligence.com/2016/04/13/is-crispr-a-solution-to-familial-amyloid-polyneuropathy/

 

http://scholar.aci.info/view/1492518a054469f0388/15411079e5a00014c3d

FAP is characterized by the systemic deposition of amyloidogenic variants of the transthyretin protein, especially in the peripheral nervous system, causing a progressive sensory and motor polyneuropathy.

FAP is caused by a mutation of the TTR gene, located on human chromosome 18q12.1-11.2.[5] A replacement of valine by methionine at position 30 (TTR V30M) is the mutation most commonly found in FAP.[1] The variant TTR is mostly produced by the liver.[citation needed] The transthyretin protein is a tetramer.    ….

 

 

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Heat Shock Proteins (HSP) and Molecular Chaperones

Curator: Larry H. Bernstein, MD, FCAP

 

HSP

 

Report on the VIIth International Symposium on Heat Shock Proteins in Biology & Medicine

The major themes of this meeting were: new properties of heat shock proteins (HSPs) and heat shock factor (HSF) and role in the etiology of cancer, molecular chaperones in aging, extracellular HSPs in inflammation and immunity, role of heat shock and the heat shock response in immunity and cancer, protein aggregation disorders and HSP expression, and Hsp70 in blood cell differentiation.
This symposium was the seventh symposium in a series presided over by Dr Stuart Calderwood aimed at exploring the association of molecular chaperones, heat shock proteins, and the heat shock response in physiological/pathological processes. The biochemistry and ultrastructure of molecular chaperones was not emphasized, as these topics are well represented at other meetings. The major themes were: new properties of heat shock proteins (HSPs) and heat shock factor (HSF) and role in the etiology of cancer, molecular chaperones in aging, extracellular HSPs in inflammation and immunity, role of heat shock and the heat shock response in immunity and cancer, protein aggregation disorders and HSP expression, and Hsp70 in blood cell differentiation. This report gives a thematic overview and does not include all the topics presented.
NEW PROPERTIES OF HSPS AND HSF, AND ROLE IN THE ETIOLOGY OF CANCER 

One of the exciting aspects of the meeting involved advances made in understanding the biology of Hsp90. In recent years, we have understood the molecular chaperone activities of Hsp90 mostly in terms of its biochemistry, cooperative interactions with cochaperones. However, Dr Len Neckers (NCI/NIH), the conference keynote speaker, has opened up new areas in our understanding of this chaperone by characterizing the role of posttranslational modification (PTM) in terms of phosphorylation, acetylation, and sumoylation in Hsp90 biology. One particularly intriguing possibility is that altered signaling mechanisms characteristic of cancer may target such PTMs, and this could contribute to the “addiction to chaperones” observed in malignant cells. (Also discussed later by Dr Mehdi Mollapour, SUNY Upstate Medical University).

In addition, interesting differences in properties of the two Hsp90 isoforms have been detected. Dr Wei Li (University of Southern California) has shown that Hsp90a can be released into the extracellular environment and there take part in cell regulation, mediating for instance wound healing effects. In addition, proteomic studies carried out by Thomas Prince (NCI/NIH) in the Neckers lab indicate that Hsp90β may be more dedicated to “housekeeping” molecular chaperone functions while Hsp90α may play more glamorous roles in cell regulation. These distinctions might not be anticipated based on the rather minimal sequence differences between the Hsp90s but offer keen insights into the biology of this chaperone. Finally, Dr Tim Haystead (Duke University) discussed the approach of targeting ectopically expressed Hsp90 for imaging and treatment.

Another PTM with implications in the stress response is the modification of intracellular proteins by monosaccharides of O-linked β-N- acetylglucosamine (O-GlcNAc). Dr Natasha Zachara (Johns Hopkins University School of Medicine) discussed targets for this modification and roles in cytoprotection.

The poster session was also rich in Hsp90 studies, mostly from the Neckers lab—presentations by Kristin Beebe et al. (NCI/NIH) Posttranslational modification state of Hsp90 differentially affects binding of small molecule inhibitors; Toshiki Kijima et al. (NCI/NIH), Defined interactions between HSF1 and Hsp90; T. Prince et al. (NCI/NIH) Hsp90 and tyrosine kinase inhibitors: A synergistic approach towards combating cancer; Andrew W. Truman (University of Chicago)Quantitive ptoteomics of the yeast Hsp70/Hsp90 interactomes during DNA damage reveals chaperonedependent regulation of ribonucleotide reductase. Inhibition of Hsp90 via Cdomain induces temporally distinct phosphorylation patterns; and Diana M. Dunn (SUNY Upstate Medical University)Phosphorylation of human Hsp90 threonine 115 modulates chaperone function and drug sensitivity.

Hsp70 is also emerging as a factor in cell regulation, exhibiting properties beyond a narrow role in chaperoning. Dr Michael Sherman (Boston University) showed a key role for Hsp72 in mammary cancer, and this property did not seem to depend on alterations in protein folding. Instead, Hsp72 appeared to function through its co-chaperone Bag3, a major regulatory molecule in cell signaling. In addition, a presentation by Stuart Calderwood (Harvard Medical School) that included work by Jianlin Gong showed that Hsp72 is required for tumor initiation and metastasis in murine spontaneous breast cancer. These effects appeared to be partially mediated through regulation of expression of the protoooncogene cMet, a key player in invasion and metastasis in cancer. We anticipate advances in understanding of the roles of individual members of the Hsp70 family, as is currently emerging for Hsp90. The prospect of targeting Hsp70 with small molecule inhibitors was elegantly discussed by Maureen Murphy (The Wistar Institute), who introduced a novel class of drugs that could selectively kill cancer cells by inhibiting Hsp70 function. In a related topic, Dr Mathias P. Mayer (University of Heidelberg) showed a detailed analysis of the activities of inhibitors targeting various domains in Hsp70.

Dr Takanori Eguchi (Harvard Medical School) then described his studies showing an unconventional role for the extracellular protease MMP3 as a nuclear protein that could trigger molecular chaperone synthesis (HspA7) in mammary cancer. Interestingly, a role in cancer for the Hsp70 co-chaperone Hsp40 was also shown by Dr Jane Trepel (NCI/NIH).

One presentation that stood apart was that of Dr Carmen Garrido (INSERM U866) who has shown very impressive studies indicating a key role for Hsp70 in hematopoiesis, acting through the factor GATA1. This role appeared to depend on nuclear localization of Hsp70, and Dr Garrido is attempting to study the role of PTM, particularly phosphorylation in this function/localization of Hsp70. This continued the theme of HSP PTM and regulation in the cell.

MOLECULAR CHAPERONES IN AGING

A symposium on molecular chaperones in aging was organized by Dr Shelley Buffenstein (University of Texas Health Science Center San Antonio). This symposium featured some fascinating studies on the naked mole rat (NMR), a rodent with a remarkable lifespan based on size (32 years compared to 3 years in the comparably sized mouse). This has permitted comparative biology studies that have uncovered important aspects of the aging process in mammals. Dr Buffenstein showed that one aspect of the proteotoxic response was enhanced in NMR—proteasome activity that was resistant to oxidative stress as well as conventional proteasome inhibitors. Such proteasome resistance appeared to be conferred by Hsp70 and Hsp40. Karl Rodriguez (also from the UTHSC San Antonio) stressed the importance of Hsp25 in the longevity of NMR. This small HSP is expressed to very high levels in this organism. Kenneth B. Storey (Carleton University) finally gave an encyclopedic presentation entitled “HeatShock Proteins and Hypometabolism in Nature”, discussing the multiple roles of chaperones in hibernation and other processes involving a step down in metabolism.

PROTEIN AGGREGATION DISORDERS AND HSP EXPRESSION

Michael Sherman (Boston University) chaired a lively and highly diverse session on protein aggregation disorders and HSPs. Gary Jones (Maynooth University) discussed his studies on the roles of Hsp104, Hsp70, and Hsp40 in prion propagation in yeast, concentrating on Hsp70. The Hsp complex was able to dissolve prions in yeast. Daniel Kaganovich (Hebrew University) then continued in a yeast theme, discussing a further strategy for resolving proteotoxic stress involving asymmetric cell division in which damaged proteins and mitochondria remain with the mother cell after mitosis. Nava Zaarur (Boston University) then discussed the role of aggresome particles in resolving aggregated proteins, in this case in eucaryotes. Alberto Macario (University of Maryland School of Medicine) discussed the role of chaperonins in proteotoxic disorders dealing with the effects of a pathogenic mutation of human CCT5 on its intrinsic properties. Dr Elaine C. Lee (University of Connecticut) discussed another type of stress. She showed significant roles for chaperones in osmotic stress responses of Caenorhabditis elegans models of polyglutamine diseases.

EXTRACELLULAR HSPS, INFLAMMATION, AND IMMUNITY

Although it is now generally accepted that HSPs can escape the confines of the cell, many questions still remain regarding their extracellular properties, particularly with regard to their immune effects. These questions include: whether HSPs are mostly immunostimulatory or immunosuppressive, whether they can induce sterile inflammation, and what structures on the immune cells recognize the HSPs. Dr Cristina Bonorino (Pontifícia Universidade Católica do Rio Grande do Sul) chaired a symposium “HSP as modulators of immunity: prokaryotic meets eukaryotic” featuring presentations by Robert Binder (University of Pittsburgh), Eckhart R. Podack (University of Miami), Renata Pasqualini (University of New Mexico Medical School), and Cristina Bonorino. In short, the talks indicated that while the prokaryotic chaperone DNA-PK can be immunosppressive and prolong the lifetime of transplanted tissues and reduce the morbidity of arthritis (Drs Bonorino and Kamal Moudgil (University of Maryland School of Medicine)), HSPs can also be immunostimulatory and act as cancer vaccines when associated with cancer antigens (Drs Binder and Podack). In the discussion, it was stressed that these effects may be related to HSP dose, with low doses of HSP antigen complex favoring immunity while higher doses may lead to immunoregulatory effects (Dr Binder). Most parties agreed that much future study is required to resolve all these issues. It was also suggested, inspired by the presentation of Dr Neckers, that HSP PTMs might also be playing roles in shading the immune effects of HSPs (Dr Bonorino). In the next session, Drs Shawn Wang (Virginia Commonwealth University School of Medicine) and John Subjeck (Roswell Park Cancer Institute) discussed the molecular foundations of their highly effective large HSP vaccines that are now in clinical trial for tumor immunotherapy. They indicated that the high avidity for antigen of the larger HSPs might be key for effectiveness. Although the nature of HSP receptors is still not fully resolved, Ayesha Murshid (Harvard Medical School) made a strong case for the scavenger receptor SREC-I as a key molecule in the effects of HSPs on immune cells. As many of the HSPs are in large families, it has not been clear whether all members of Hsp90 or Hsp70 can function outside the cell. Dr Wei Li (University of Southern California) showed that HSP90 family member Hsp90α is the major secreted factor while Dr John Williams (University of Chester) showed potent extracellular effects for human HSP70 isoform HSPA1A. Extracellular roles are not restricted to Hsp90, and Edward O’Brien (Libin Cardiovascular Institute of Alberta/University of Calgary) discussed the extracellular role of heat shock protein 27 (HSPB1) in inflammatory vascular disease. Another lively issue is whether HSPs are released as free proteins, packaged in exosomes, or whether both forms co-exist. This issue was discussed by Monika Fleshner (University of Colorado) and Antonio De Maio (University of California San Diego). Dr De Maio brought up the interesting scenario of Hsp70 binding directly to lipid membranes and perhaps forming membrane channels (Ryan White, University of Maryland).

HSPs are evidently not the only types of stress proteins that can function in the extracellular milieu, as indicated by Dr Michael A. Lynes (University of Connecticut). In a presentation entitled Therapeutic manipulation of the stress response during inflammatory disease, Dr Lynes showed a significant role for extracellular metallothionen in inflammatory bowel disease. Along those lines, Dr George Perdrizet (University of California San Diego) discussed the use of hyperbaric oxygen for enhanced wound healing in diabetic neuropathy, showing impressive clinical findings.

see more at — doi:  10.1007/s12192-014-0562-z

Lens Intermediate Filaments

 The ocular lens assembles two separate Intermediate Filament systems sequentially with differentiation. Canonical 8–11 nm IFs composed of Vimentin are assembled in lens epithelial cells and younger fiber cells, while the fiber cell-specific Beaded Filaments are switched on as fiber cell elongation initiates. Some of the key features of both filament systems are reviewed. Actin filaments and microtubules are essential to the most elemental functions of eukaryotic cells. These filamentous structures are assembled from proteins derived from small, highly conserved gene families. Though tissue specificity exists in the expression of some actin and tubulin family members, they are generally expressed in a ubiquitous manner, and are required for eukaryotic cell survival and replication. In contrast, the family of proteins that comprise the cytoplasmic Intermediate Filaments (IFs) is one of the largest in the human genome with greater than 60 members. IFs are generally not required for cell survival, and are absent from single cell eukaryotes, suggesting a more recent appearance on the evolutionary stage, and a less-essential role in the biology of the cell.
The IF family also differs sharply from actins and tubulins in that there is great variation in both size and sequence among the IF proteins, with sequence identity falling below 30% between more distant members of the human IF family. However, despite the large number of IF proteins available for the construction of IFs, any given cell typically expresses only 1–3 IF proteins, with expression tightly restricted to cell type and state of differentiation. This suggests a considerable degree of cell-specific specialization.
While IF proteins show considerable sequence and size variation, they are unified into a family on the basis of three major features:
1. Predicted domain structure (see figure 1): Algorithms that predict coiled-coil structure show a common predicted domain structure consisting of a) head and tail domains which are quite variable in both size and sequence, and b) a central rod domain where the size (~310 amino acids) and predicted secondary structure is strongly conserved. The rod domain consists of large regions of alpha helical structure (coil domains) interrupted by short non-helical regions (“linkers”) that connect the coil domains. The size, number, and placement of linkers and coils are well-conserved. Moreover, the coil domains exhibit a heptad repeat pattern where the 1, 4 positions in the heptad are dominated by hydrophobic amino acids. Because the 1,4 positions are aligned on one  side of the helix, they form a largely hydrophobic “stripe” that runs along one side of the alpha helix. This stripe mediates the dimerization of two matched coil domains. The hydrophobic stripe gently twists around the axis of the helix, giving rise to a supercoiling of two alpha helices, hence the “coiled-coil”.
The requisite hydrophobicity at the 1, 4 positions of the heptad can be conferred by any of several amino acids, thus the central rod domain of IF proteins, while showing conserved secondary structure, also exhibits a generally high degree of sequence variation. The exceptions to this are two short motifs found at either end of the central rod domain, commonly called the Helix Initiation Motif (HIM) and the Helix termination Motif (HTM). At these two sites the primary sequence among IF proteins is well conserved. Not surprisingly, the HIM and HTM motifs are intolerant of mutations, with the majority of known IF diseases arising from point mutations in these sites (http://www.interfil.org).
2. Conserved gene structure: Sequence analysis of IF proteins has allowed clustering of IF proteins into several major classes. Sequence conservation in the rod domain is high within a class (typically greater than 70%) but low between classes. Analysis of the IF genes shows that there is conservation of gene structure as well within the IF family, with the number and placement of introns and exons well conserved, especially in the central rod domain. The degree of gene structure conservation correlates well with the degree of primary sequence conservation, and reinforces the grouping of IF proteins into classes on the basis of primary sequence.
The Type I and II IF classes are called cytokeratins, and these comprise the IFs of epithelia. These begin assembly as an obligate heterodimer of one Type I and one Type II cytokeratin. The Type III IF proteins include vimentin, desmin, GFAP, and peripherin, and these are commonly found in tissues of mesenchymal origin. While Type III IF proteins can heterodimerize, they are more commonly found as homomeric filaments. The Type IV IF proteins are the neurofilament proteins Heavy (NFH), Medium (NFM) and Light (NFL), which assemble collectively into the IFs of neurons.
3. IF proteins form 8–11 nm diameter IFs. Ultimately, despite the differences in head/ tail size and sequence, and variation in the rod domain sequence, all cytoplasmic IF proteins typically assemble into 8–11 nm IFs.
The mechanism by which vimentin is removed as the cell transitions to the organelle-free state is unknown. In cells undergoing mitosis, vimentin IFs are routinely dismantled by phosphorlylation (Inagaki, Nishi et al. 1987), a modification that causes the relatively stable IF polymer break up into smaller subunits, thought to be tetramers. These are subsequently reassembled after cell division is complete. However, vimentin in lens fiber cells appears to removed, and not simply dismantled. IFs are known to be among the first targets of calcium activated proteases (calpains) in cells that are damaged, and many investigators have demonstrated the calcium-activated degradation of both vimentin and BFs in lens(Yoshida, Murachi et al. 1984; Truscott, Marcantonio et al. 1990; Marcantonio and Duncan 1991; Bettelheim, Qin et al. 1995; Andersson, Sjostrand et al. 1996; Sanderson, Marcantonio et al. 1996; Sanderson, Marcantonio et al. 2000). The dismantling of organelles implies a potential release of calcium from organelles in which it is otherwise routinely sequestered. Whether this release occurs, and whether it alters cytoplasmic calcium levels to a degree that would activate those calpains present in the fiber cell is not known.
Caspases activated in the apoptotic cascade can target conserved sites in IF proteins(Caulin, Salvesen et al. 1997). The elimination of organelles from the fiber cell represents an incomplete apoptotic event, and thus those enzymes responsible for organelle elimination may also represent a viable mechanism for explanation of vimentin’s suggested disappearance(Oshima 2002; Omary, Coulombe et al. 2004).
The loss or reduction of vimentin levels does not leave the mature lens fiber cell devoid of an IF system, however. In a manner that emulates IF switching seen in stratified epithelia, a second generation IF system is switched on in the lens as vimentin is being switched off. It is here where the story of the lens IF system takes the most unusual turn yet described in the IF field.
The initial recognition that the mature lens fiber cells departed from the IF dogma was made when Maisel and co-workers noted the presence of “Beaded Chain Filaments” or Beaded Filaments (BFs) in an electron microscopic analysis of chick lens homogenates (Maisel and Perry 1972; Maisel 1977; Bradley and Maisel 1978; Bradley, Ireland et al. 1979). These studies noted a clearly filamentous structure that was distinct from thin filaments, microtubules, and IFs, which at that time were emerging as the universal cytoskeletal structures common to essentially all vertebrate cells. Speculation emerged that these structures were thin filaments with bound alpha crystallin particles, or nucleosomes on DNA, but these explanations were ruled out experimentally (Bloemendal, Berbers et al. 1984; Ireland and Maisel 1984).
Consistent with the emerging role of IFAPs in modulating and adapting IF function is the observation that fiber cell vimentin IFs interact with the N Cadherin-gamma catenin complex (Leonard, Chan et al. 2008), lengsin(Wyatt, Gao et al. 2008), MIP(Lindsey Rose, Gourdie et al. 2006), periplakin(Yoon and FitzGerald 2008), tropomodulin(Fischer, Quinlan et al. 2003) and possibly other complexes which are present in lens(Bagchi, Katar et al. 2002; Straub, Boda et al. 2003; Bagchi, Katar et al. 2004). The number of candidate linker proteins demonstrated in lens leads to the expectation that the BF and IF are likely to accomplish multiple functions, and that these may be modulated as differentiation progresses, and as the fiber cell proteome changes, either by expression or proteolysis. Similarly, the small heat shock proteins, whose chaperone function appears essential to IF/BF assembly and maintenance, must be considered as critical parts of the biology of IFs in lens. Mutations in the small heat shock proteins have been shown to precipitate a failure in the IF systems in many tissues, and in lens specifically, and to subsequently emulate IF diseases (FitzGerald and Graham 1991; Nicholl and Quinlan 1994; Carter, Hutcheson et al. 1995; Vicart, Caron et al. 1998; Muchowski, Valdez et al. 1999; Perng, Cairns et al. 1999; Perng, Muchowski et al. 1999; Evgrafov, Mersiyanova et al. 2004; Treweek, Rekas et al. 2005; Song, Hanson et al. 2008). The growing multiplicity of IF interactions underscores the need to expect that failure in “IF function” in the lens can result from failure in a wide spectrum of proteins that affect assembly, phosphorylation, proteolytic modification, stability, removal, or linkage to other cellular structures, and that “IF failure” is likely to show considerable variability in phenotype.

Morphological characterization of the AlphaA- and AlphaB-crystallin double knockout mouse lens    Edited by Harry Maisel

Daniel L BoyleLarry TakemotoJames P Brady and Eric F Wawrousek
BMC Ophthalmology 2003; 3:3   http://dx.doi.org:/10.1186/1471-2415-3-3

Background: One approach to resolving some of the in vivo functions of alpha-crystallin is to generate animal models where one or both of the alpha-crystallin gene products have been eliminated. In the single alpha-crystallin knockout mice, the remaining alpha-crystallin may fully or partially compensate for some of the functions of the missing protein, especially in the lens, where both alphaA and alphaB are normally expressed at high levels. The purpose of this study was to characterize gross lenticular morphology in normal mice and mice with the targeted disruption of alphaA- and alphaB-crystallin genes (alphaA/BKO). Methods: Lenses from 129SvEvTac mice and alphaA/BKO mice were examined by standard scanning electron microscopy and confocal microscopy methodologies. Results: Equatorial and axial (sagittal) dimensions of lenses for alphaA/BKO mice were significantly smaller than age-matched wild type lenses. No posterior sutures or fiber cells extending to the posterior capsule of the lens were found in alphaA/BKO lenses. Ectopical nucleic acid staining was observed in the posterior subcapsular region of 5 wk and anterior subcapsular cortex of 54 wk alphaA/BKO lenses. Gross morphological differences were also observed in the equatorial/bow, posterior and anterior regions of lenses from alphaA/BKO mice as compared to wild mice. Conclusion: These results indicated that both alphaA- and alphaB-crystallin are necessary for proper fiber cell formation, and that the absence of alpha-crystallin can lead to cataract formation.

Dogfish a-Crystallin Sequences COMPARISON WITH SMALL HEAT SHOCK PROTEINS AND SCHISTOSOMA EGG ANTIGEN*

Wilfried W. de JongS, Jack A. M. Leunissen, Pieter J. M. Leenen, Anneke Zweers, and Marlies Versteeg
J BIOL CHEM  1988; 263(11):5141-5149

The amino acid sequences of the a-crystallin A and B chains of the dogfish, Squalus acanthias, have been determined. Comparison with a-crystallins from other species reveals that charged amino acid replacements have been strongly avoided in the evolution of this lens protein. The homology of a-crystallins with the small heat shock proteins is pronounced throughout the major part of the proteins, starting from the position of the first intron in the a-crystallin genes, but is also detectable in the amino-terminal sequences of human, Xenopus, and Drosophila small heat shock proteins. In addition, a remarkable short sequence similarity is present only in the amino termini of dogfish aB and Drosophila HSP22. The Schistosoma egg antigen p40 turns out to have a tandomly repeated region of homology with the common sequence domain of a-crystallins and small heat shock proteins. Comparison of hydropathy profiles indicates the conservation of conformation of the common domains in these three families of proteins. Construction of phylogenetic trees suggests that the aA and aB genes apparently originated from a single ancestral small heat shock protein gene and indicates that introns have been lost during the evolution of the heat shock protein.

Acknowledgment – Maisel, H. (ed) (1985) The Ocular Lens, Marcel Dekker, New. York

 

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Brain Biobank and studies of disease structure correlates

Larry H. Bernstein, MD, FCAP, Curator

LPBI

 

Unveiling Psychiatric Diseases

Researchers create neuropsychiatric cellular biobank

Image: iStock/mstroz
Image: iStock/mstroz
Researchers from Harvard Medical School and Massachusetts General Hospital have completed the first stage of an important collaboration aimed at understanding the intricate variables of neuropsychiatric disease—something that currently eludes clinicians and scientists.

The research team, led by Isaac Kohane at HMS and Roy Perlis at Mass General, has created a neuropsychiatric cellular biobank—one of the largest in the world.

It contains induced pluripotent stem cells, or iPSCs, derived from skin cells taken from 100 people with neuropsychiatric diseases such as schizophrenia, bipolar disorder and major depression, and from 50 people without neuropsychiatric illness.

In addition, a detailed profile of each patient, obtained from hours of in-person assessment as well as from electronic medical records, is matched to each cell sample.

As a result, the scientific community can now for the first time access cells representing a broad swath of neuropsychiatric illness. This enables researchers to correlate molecular data with clinical information in areas such as variability of drug reactions between patients. The ultimate goal is to help treat, with greater precision, conditions that often elude effective management.

The cell collection and generation was led by investigators at Mass General, who in collaboration with Kohane and his team are working to characterize the cell lines at a molecular level. The cell repository, funded by the National Institutes of Health, is housed at Rutgers University.

“This biobank, in its current form, is only the beginning,” said Perlis, director of the MGH Psychiatry Center for Experimental Drugs and Diagnostics and HMS associate professor of psychiatry. “By next year we’ll have cells from a total of four hundred patients, with additional clinical detail and additional cell types that we will share with investigators.”

A current major limitation to understanding brain diseases is the inability to access brain biopsies on living patients. As a result, researchers typically study blood cells from patients or examine post-mortem tissue. This is in stark contrast with diseases such as cancer, for which there are many existing repositories of highly characterized cells from patients.

The new biobank offers a way to push beyond this limitation.

 

A Big Step Forward

While the biobank is already a boon to the scientific community, researchers at MGH and the HMS Department of Biomedical Informatics will be adding additional layers of molecular data to all of the cell samples. This information will include whole genome sequencing and transcriptomic and epigenetic profiling of brain cells made from the stem cell lines.

Collaborators in the HMS Department of Neurobiology, led by Michael Greenberg, department chair and Nathan Marsh Pusey Professor of Neurobiology,  will also work to examine characteristics of other types of neurons derived from these stem cells.

“This can potentially alter the entire way we look at and diagnose many neuropsychiatric conditions,” said Perlis.

One example may be to understand how the cellular responses to medication correspond to the patient’s documented responses, comparing in vitro with in vivo. “This would be a big step forward in bringing precision medicine to psychiatry,” Perlis said.

“It’s important to recall that in the field of genomics, we didn’t find interesting connections to disease until we had large enough samples to really investigate these complex conditions,” said Kohane, chair of the HMS Department of Biomedical Informatics.

“Our hypothesis is that here we will require far fewer patients,” he said. “By measuring the molecular functioning of the cells of each patient rather than only their genetic risk, and combining that all that’s known of these people in terms of treatment response and cognitive function, we will discover a great deal of valuable information about these conditions.”

Added Perlis, “In the early days of genetics, there were frequent false positives because we were studying so few people. We’re hoping to avoid the same problem in making cellular models, by ensuring that we have a sufficient number of cell lines to be confident in reporting differences between patient groups.”

The generation of stem cell lines and characterization of patients and brain cell lines is funded jointly by the the National Institute of Mental Health, the National Human Genome Research Institute and a grant from the Centers of Excellence in Genomic Science program.

 

On C.T.E. and Athletes, Science Remains in Its Infancy

Se Hoon ChoiYoung Hye KimMatthias Hebisch, et al.

http://www.nature.com/articles/nature13800.epdf

Alzheimer’s disease is the most common form of dementia, characterized by two pathological hallmarks: amyloid-β plaques and neurofibrillary tangles1. The amyloid hypothesis of Alzheimer’s disease posits that the excessive accumulation of amyloid-β peptide leads to neurofibrillary tangles composed of aggregated hyperphosphorylated tau2, 3. However, to date, no single disease model has serially linked these two pathological events using human neuronal cells. Mouse models with familial Alzheimer’s disease (FAD) mutations exhibit amyloid-β-induced synaptic and memory deficits but they do not fully recapitulate other key pathological events of Alzheimer’s disease, including distinct neurofibrillary tangle pathology4, 5. Human neurons derived from Alzheimer’s disease patients have shown elevated levels of toxic amyloid-β species and phosphorylated tau but did not demonstrate amyloid-β plaques or neurofibrillary tangles6, 7, 8, 9, 10, 11. Here we report that FAD mutations in β-amyloid precursor protein and presenilin 1 are able to induce robust extracellular deposition of amyloid-β, including amyloid-β plaques, in a human neural stem-cell-derived three-dimensional (3D) culture system. More importantly, the 3D-differentiated neuronal cells expressing FAD mutations exhibited high levels of detergent-resistant, silver-positive aggregates of phosphorylated tau in the soma and neurites, as well as filamentous tau, as detected by immunoelectron microscopy. Inhibition of amyloid-β generation with β- or γ-secretase inhibitors not only decreased amyloid-β pathology, but also attenuated tauopathy. We also found that glycogen synthase kinase 3 (GSK3) regulated amyloid-β-mediated tau phosphorylation. We have successfully recapitulated amyloid-β and tau pathology in a single 3D human neural cell culture system. Our unique strategy for recapitulating Alzheimer’s disease pathology in a 3D neural cell culture model should also serve to facilitate the development of more precise human neural cell models of other neurodegenerative disorders.

 

 

Figure 2: Robust increases of extracellular amyloid-β deposits in 3D-differentiated hNPCs with FAD mutations.close

Robust increases of extracellular amyloid-[bgr] deposits in 3D-differentiated hNPCs with FAD mutations.

a, Thin-layer 3D culture protocol. HC, histochemistry; IF, immunofluorescence; IHC, immunohistochemistry. b, Amyloid-β deposits in 6-week differentiated control and FAD ReN cells in 3D Matrigel (green, GFP; blue, 3D6; scale bar, …

 

Stem Cell-Based Spinal Cord Repair Enables Robust Corticospinal Regeneration

 

Novel use of EPR spectroscopy to study in vivo protein structure

http://www.news-medical.net/whitepaper/20160315/Novel-use-of-EPR-spectroscopy-to-study-in-vivo-protein-structure.aspx

α-synuclein

α-synuclein is a protein found abundantly throughout the brain. It is present mainly at the neuron ends where it is thought to play a role in ensuring the supply of synaptic vesicles in presynaptic terminals, which are required for the release of neurotransmitters to relay signals between neurons. It is critical for normal brain function.

However, α-synuclein is also the primary protein component of the cerebral amyloid deposits characteristic of Parkinson’s disease and its precursor is found in the amyloid plaques of Alzheimer’s disease. Although α-synuclein is present in all areas of the brain, these disease-state amyloid plaques only arise in distinct areas.

Alpha-synuclein protein. May play role in Parkinson’s and Alzheimer’s disease.  © molekuul.be / Shutterstock.com

Imaging of isolated samples of α-synuclein in vitro indicate that it does not have the precise 3D folded structure usually associated with proteins. It is therefore classed as an intrinsically disordered protein. However, it was not known whether the protein also lacked a precise structure in vivo.

There have been reports that it can form helical tetramers. Since the 3D structure of a biological protein is usually precisely matched to the specific function it performs, knowing the structure of α-synuclein within a living cell will help elucidate its role and may also improve understanding of the disease states with which it is associated.

If α-synuclein remains disordered in vivo, it may be possible for the protein to achieve different structures, and have different properties, depending on its surroundings.

Techniques for determining protein structure

It has long been known that elucidating the structure of a protein at an atomic level is fundamental for understanding its normal function and behavior. Furthermore, such knowledge can also facilitate the development of targeted drug treatments. Unfortunately, observing the atomic structure of a protein in vivo is not straightforward.

X-ray diffraction is the technique usually adopted for visualizing structures at atomic resolution, but this requires crystals of the molecule to be produced and this cannot be done without separating the molecules of interest from their natural environment. Such processes can modify the protein from its usual state and, particularly with complex structures, such effects are difficult to predict.

The development of nuclear magnetic resonance (NMR) spectroscopy improved the situation by making it possible for molecules to be analyzed under in vivo conditions, i.e. same pH, temperature and ionic concentration.

More recently, increases in the sensitivity of NMR and the use of isotope labelling have enabled determinations of the atomic level structure and dynamics of proteins to be determined within living cells1. NMR has been used to determine the structure of a bacterial protein within living cells2 but it is difficult to achieve sufficient quantities of the required protein within mammalian cells and to keep the cells alive for NMR imaging to be conducted.

Electron paramagnetic resonance (EPR) spectroscopy for determining protein structure

Recently, researchers have managed to overcome these obstacles by using in-cell NMR and electron paramagnetic resonance (EPR) spectroscopy. EPR spectroscopy is a technique that is similar to NMR spectroscopy in that it is based on the measurement and interpretation of the energy differences between excited and relaxed molecular states.

In EPR spectroscopy it is electrons that are excited, whereas in NMR signals are created through the spinning of atomic nuclei. EPR was developed to measure radicals and metal complexes, but has also been utilized to study the dynamic organization of lipids in biological membranes3.

EPR has now been used for the first time in protein structure investigations and has provided atomic-resolution information on the structure of α-synuclein in living mammalians4,5.

Bacterial forms of the α-synuclein protein labelled with 15N isotopes were introduced into five types of mammalian cell using electroporation. Concentrations of α-synuclein close to those found in vivo were achieved and the 15N isotopes allowed the protein to be clearly defined from other cellular components by NMR. The conformation of the protein was then determined using electron paramagnetic resonance (EPR).

The results showed that within living mammalian cells α-synuclein remains as a disordered and highly dynamic monomer. Different intracellular environments did not induce major conformational changes.

Summary

The novel use of EPR spectroscopy has resolved the mystery surrounding the in vivo conformation of α-synuclein. It showed that α-synuclein maintains its disordered monomeric form under physiological cell conditions. It has been demonstrated for the first time that even in crowded intracellular environments α-synuclein does not form oligomers, showing that intrinsic structural disorder can be sustained within mammalian cells.

References

  1. Freedberg DI and Selenko P. Live cell NMR Annu. Rev. Biophys. 2014;43:171–192.
  2. Sakakibara D, et al. Protein structure determination in living cells by in-cell NMR spectroscopy. Nature 2009;458:102–105.
  3. Yashroy RC. Magnetic resonance studies of dynamic organisation of lipids in chloroplast membranes. Journal of Biosciences 1990;15(4):281.
  4. Alderson TA and Bax AD. Parkinson’s Disease. Disorder in the court. Nature 2016; doi:10.1038/nature16871.
  5. Theillet FX, et al. Structural disorder of monomeric α-synuclein persists in mammalian cells. Nature 2016; doi:10.1038/nature16531.

 

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Deciphering Mode of Action of Functionally Important Regions

Larry H. Bernstein, MD, FCAP, Curator

LPBI

 

Deciphering Mode of Action of Functionally Important Regions in the Intrinsically Disordered Paxillin (Residues 1-313) Using Its Interaction with FAT (Focal Adhesion Targeting Domain of Focal Adhesion Kinase)

Intrinsically disordered proteins (IDPs) play a major role in various cellular functions ranging from transcription to cell migration. Mutations/modifications in such IDPs are shown to be associated with various diseases. Current strategies to study the mode of action and regulatory mechanisms of disordered proteins at the structural level are time consuming and challenging. Therefore, using simple and swift strategies for identifying functionally important regions in unstructured segments and understanding their underlying mechanisms is critical for many applications. Here we propose a simple strategy that employs dissection of human paxillin (residues 1–313) that comprises intrinsically disordered regions, followed by its interaction study using FAT (Focal adhesion targeting domain of focal adhesion kinase) as its binding partner to retrace structural behavior. Our findings show that the paxillin interaction with FAT exhibits a masking and unmasking effect by a putative intra-molecular regulatory region. This phenomenon suggests how cancer associated mutations in paxillin affect its interactions with Focal Adhesion Kinase (FAK). The strategy could be used to decipher the mode of regulations and identify functionally relevant constructs for other studies.
Neerathilingam M, Bairy SG, Mysore S (2016) Deciphering Mode of Action of Functionally Important Regions in the Intrinsically Disordered Paxillin (Residues 1-313) Using Its Interaction with FAT (Focal Adhesion Targeting Domain of Focal Adhesion Kinase). PLoS ONE 11(2): e0150153. doi:10.1371/journal.pone.0150153

Genomic data suggests that a large proportion of eukaryotic proteins appear to adopt disordered structures in physiological conditions [1, 2]. Mutations/modifications in such IDPs are shown to be associated with various diseases (like cancer) [3]; therefore, understanding their structural behavior is critical for various applications like drug-targeting, mapping protein interactions, deciphering mode of action and finding functional relevance. However, deciphering mode of action in IDPs has been challenging given that unstructured segments render poor chemical shift dispersions and electron density in major techniques like NMR and X-ray, respectively [4]. For example, it took almost 10 years to decipher the mode of action of Sic1, a disordered protein involved in inhibition of a cyclin-dependent kinase [5]. One way to map and study the functional regions is to make truncated constructs by dissecting the whole construct rationally. A limited number of dissection constructs are usually generated; this is due to the time-consuming and challenging process of generating soluble and functionally relevant constructs when studies are performed in-vivo and constructs are prepared and tested sequentially. Here we present a simple high throughput (HTP) screening strategy (Fig 1a), which focuses on finding functionally relevant regions in IDPs based upon its interaction with a binding partner. Close to thirty dissection constructs of the IDP were generated and studied in parallel to understand the importance and functionality of the various regions of the protein. We perform cell-free expression followed by solubility check and GST pull-down interaction study in HTP format. Though both cell-free expression and GST pull-down assay have been individually performed in HTP format [6, 7], we did not find previous studies that combine the two methods in HTP format. Although the nature of interaction of IDPs with respective binding partners may vary, our strategy may be used to derive crucial insights into “structural behavior” of the unstructured segments in modulating the interaction. The strategy can also be used to identify functionally important regions in the IDP that would be suitable for further structural studies.

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Fig 1. Dissection of paxillin constructs (residues 1–313) followed by expression and interaction studies.

(a) Timeline for overall-strategy. (b) Illustration of solubility and activity level of linear dissected human paxillin (residues 1–313). (c) Phosphor screen image of filter assay for optimization of temperature for paxillin constructs (left). Tabular representation of paxillin constructs, negative and positive controls corresponding to each well in filter assay [1].(d) Phosphor screen image of 10% SDS PAGE of 35S labeled cell-free expressed samples after GST pull-down assay of the paxillin constructs A1–E1; The right panel shows fraction of interaction of each construct with respect to B2 (since B2 showed maximum level of interaction) (e) Illustration of solubility and activity of dissected C3 constructs. All experiments were performed in triplicates and averaged. To rule out non-specific interactions that might occur with GST tagged FAT, GFP that was expressed in cell-free system and a reaction without DNA template were used as negative controls.    http://dx.doi.org:/10.1371/journal.pone.0150153.g001

Disorder/Intrinsic disorder seems to be a common feature of hub proteins in eukaryotes [2], thus highlighting the need for studying the mode of action of unstructured segments in such proteins. Here we used paxillin (residues 1–313), an intrinsically disordered construct, for demonstrating this approach. Paxillin (residues 1–313) consists of multiple protein interaction sites that are connected by flexible disordered sequences [8]. The disordered regions in paxillin have been detrimental in efforts to study the complete structure of the protein due to the demerits mentioned previously. This explains the lack of structural details of regulation of paxillin binding. Residues 1–313 of paxillin consist of five leucine-rich sequences LD1-LD5 (with consensus sequence: LDXLLXXL), termed LD motifs, which are highly conserved between species and other family members such as Hic-5, leupaxin and PAXB [8]. Paxillin interacts with multiple proteins involved in cell migration, actin rearrangements and cell proliferation [9]. Mutations in paxillin are shown to be associated with lung cancer [3, 10]; and the differential expression of paxillin is associated with various forms of cancer and other diseases such as Alzheimer’s and inflammation [1113]. This implies the importance of studying the structural and functional characteristics of paxillin. Most paxillin studies focus on interactions of LD motifs with proteins such as focal adhesion kinase (FAK), vinculin and v-crk, providing clues towards their importance in deciphering the functionality of paxillin [8, 14, 15]. Though regions of paxillin that bind to various partners were deciphered through previous studies, the basis of effect of mutations in paxillin on binding its partners was not explained. Mutations in paxillin, some that were observed to be associated with cancer were positioned in the intrinsically disordered regions between the LD motifs and not on the motifs themselves [3, 10]. For example, P30S, G105A and A127T mutations lie between LD1 and LD2 motif; P233L and T255I mutations lie between LD3 and LD4 motifs. This shows that the LD motifs alone do not govern the functionality, but unstructured regions linking the LD motifs could play a major role. In normal conditions, FAT (Focal adhesion targeting domain of FAK) binds hydrophobically through its HP1 (Hydrophobic patch 1) and HP2 (Hydrophobic patch 2) sites to paxillin LD motifs—LD2 and LD4 [16, 17], which lead to activation of binding sites for other proteins on paxillin. LD2 preferentially binds to the HP2 site, whereas LD4 preferentially binds to the HP1 site [18]. In a state of cancer caused by mutations in paxillin, the LD interactions could be hindered, as mutations in the unstructured segments result in abnormal binding of FAK to either of the LD motifs [9]. Here we wanted to locate the region involved in the structural modulation of paxillin-FAT interaction by adopting a simple approach (Fig 1) that involves dissected proteins generated using cell-free protein expression coupled with protein-protein interaction study. We map the disordered proteins’ structural importance to understand the function and modulation of paxillin-FAT interaction in days rather than months (Fig 1a).

Dissection and identification of fragments of paxillin (residues 1–313) with functional relevance

We dissected paxillin (residues 1–313) (Fig 1b) into nested sets using PCR such that each of the constructs had either or both LD2 and LD4 motifs (S1 Fig and S1 Table). Further, these constructs were expressed in soluble form using small-scale cell-free expression system in a 96 well format (Fig 1c). However, all constructs except A6, B6, C4 and C5 expressed detectable amounts of protein (S2a Fig and S2 Table). The failure in expression of the above constructs could be due to the instability of the smaller peptide fragments that might be susceptible to proteolytic cleavage [19]. Soluble protein from small-scale expression of the dissected constructs namely A1, A2, A3, A4, A5, B1, B2, B3, B4, B5, C1, C2, C3, D1, D2, and E1 were pulled down and analysed (Fig 1d). Although constructs A1–A5, B1–B5, C1, C2, D1 and E1 interacted successfully, C3 (containing LD2) and D2 (containing LD4) failed to interact (Fig 2c) despite containing LD motifs. However, based on previous reports [8, 16, 17], we expected all constructs containing either LD2 and/or LD4 to interact with the FAT domain. Therefore, this led us to suspect that intra-molecular auto-inhibition in unstructured segments modulated binding of FAT to LD motifs in paxillin.

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Fig 2. Regulatory and masking regions around paxillin’s LD2 and LD4 and their circular dichroism spectra.

(a) CD spectra of paxillin LD peptides (LD1-LD5) and constructs: B2, C3, C35 and D2. CD spectra of LD2, LD4, C35 and D2 constructs showed negative bands at 222nm and 206nm and a positive band at 192nm that confirms the presence of alpha helical content thus may behave as folded effector binding sites. However, LD1, LD3, LD5, B2 and C3 do not show the characteristic peaks of secondary structures, thus may behave as unfolded effector binding sites. (b) LD2 regulatory region (54–130) and masking region (167–224) evidenced by constructs B3, B4 and B5. (c) LD4 regulatory region (216–257) and masking region (280–313) evidenced by constructs D1, D2 and E1.
http://dx.doi.org:/10.1371/journal.pone.0150153.g002

Identification of regulatory regions and their mechanisms

To investigate the non-interaction of C3, a series of C3 deleted constructs (C31 –C310) (Fig 1e,S1 Table) were generated to determine the internal region that influenced the non-functioning of C3. C36 linear template could not be amplified for expression. As solubility of C3 could play a critical role in determining interaction, the homogeneity of the sample was confirmed by capillary electrophoresis under non-reducing conditions [20] (See S3 Fig). The linear templates—C31, C32, C33, C34 and C35 were successfully expressed in soluble form, The other C3 deleted constructs did not express due to issues related to small size as described earlier. Surprisingly, none of the C3 deleted constructs interacted with FAT despite the presence of the LD2 motif, although constructs such as B3, B4 and B5 that contain regions overlapping with C3 showed interaction (S2b and S2c Fig, Fig 1d and 1e). Here B3 that included the whole of C3 and unstructured segment 54–130 showed interaction (Fig 1b). Constructs B4 and B5 also containing residues 54–130 showed interaction despite differing from B3 by lacking regions 167–224 and 155–224, respectively. Interestingly, the non-interacting constructs C3 and C35 do not contain 54–130 residues, but include the regions 167–224 and 167–189, respectively (Fig 1b). Here constructs containing region 167–189 but lacking 54–130 did not interact with FAT despite LD motif alone showing interaction (switch off) (Fig 3a). Whereas, if 54–130 was included, interaction was reinstated (switch on) (Fig 3a). This clearly shows that interaction of LD2 in construct C35 is masked by residues 167–189 (masking region) (Fig 2b). The constructs B3 and B4 binding to FAT despite the presence of the masking region led us to conclude that the region 54–130 (regulatory region) acts to remove the masking effect (Fig 2b).
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Fig 3. Binding studies of paxillin constructs using Bio-layer Interferometry on OctetRed96.

(a) Switch off in C3 and D2 on LD2 and LD4 respectively; Hypothesis of partial switch on when regulatory region of LD2 is absent, as evidenced in C2. (b) Concentration calibration curves depicting binding of constructs B2, C35, ‘54–189’, ‘79–189’, ‘105–189’ with GST-FAT. The data is representative of a single experiment. Each experiment was performed at-least thrice. (c) Illustrations of C35, C35_1, C35_2 and C35_3.  http://dx.doi.org:/10.1371/journal.pone.0150153.g003

Similar to LD2, LD4 in construct D2 containing 216–257 (masking region) requires additional residues of paxillin 280–313 (regulatory region) for FAT binding (Fig 2c), which was demonstrated by showing the interaction with constructs D1 (spanning region 216–313) (Fig 1b) and E1 (spanning region 258–313). To visualize the non-binding of FAT to C35, in-silico methods were employed to model the C35 construct and docked with the crystal structure of FAT (1K05, residues 916–1050 [21]) (Fig 4). The docking results showed a clear masking effect in the C35 construct by the 167–189 (masking region) residues. The constructs B2, C3 and C35 were also structurally characterized using CD analysis (Large scale cell-free expression was performed for this purpose, see S3 Fig). The percentage of alpha helical content was found to be much higher in C35 (95.32%) as compared to B2 (12.43%) (Fig 2a, S3 Table). Therefore, the dissection(s) of B2 to C35 allowed the identification of structured regions (C35) as compared to the disordered B2. Further, it showed that the LD2 peptide and C35 have significant alpha-helical structures that do not translate into functional similarity as evidenced by the inability of C3, C35 and D2 to bind to FAT. Moreover, LD2 peptide binds to FAT while C35 does not (Fig 1e and S2b and S2c Fig). A similar observation was made when comparing the ability of LD4 peptide and the inability of D2 to bind to FAT despite both having detectable α-helical content (Fig 1b). Thus, these results confirm the existence of masking and regulatory regions (Fig 2b and 2c) that determine switch on and off and in turn, intra-molecular auto-inhibition. C2 showed activity despite missing regulatory regions for both LD2 and LD4 (similar activity observed in C1). This could be because the unfolded nature of LD3 effector binding site that is located between LD2 and LD4 is flexible to mask only a single LD motif but not both (Partial switch on, Fig 3a).

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Fig 4. In-silico analysis of non-binding of C35.

(a) LD2 crystal structure from PDB id: 1K05 (left) being compared with the LD2 structure in the side view and top view of C35 structure showing the masking of the hydrophobic binding region predicted through HMM based SAM-T08 software. The LD2 binding region and the masking regions are depicted by the bracketed region. (b) Docking control showing FAT (co-ordinates from PDB id: 1K05) and LD2 (co-ordinates from PDB id: 2L6F, NMR model # 1) interaction using Hex 6.3 software. (c) Docking of C35 with FAT showing non-interaction due to masking effect. The sidechains of the active residues are shown as red sticks. The hydrophobic patch—HP2 in FAT molecule, which preferentially binds to LD2 is shown as a space filling model in orange (part of helix 1 of FAT) and grey (part of helix 4 of FAT) colors.   http://dx.doi.org:/10.1371/journal.pone.0150153.g004

To predict the influence of this structural modulation, the state of LD motifs structurally before and after binding to FAT had to be understood. CD spectra of LD1, LD3 and LD5 peptides showed characteristics of random coil (Fig 2a, S3 Table) thus validating that the LD1, LD3 and LD5 motifs could exist as unfolded effector binding sites (not available for interaction) in our study and could fold upon undergoing allosteric changes after binding to their respective targets.

Validation of protein-protein interaction study using bio-layer interferometry studies

Bio-layer interferometry studies were performed to further validate the interaction studies and also to get insights into the binding affinities. Here apart from constructs B2 and C35, three other constructs that include different lengths of the regulatory region along with the C35 region were used for the studies, namely—Construct C35_1(54–189); Construct C35_2 (79–189) and Construct C35_3 (105–189) (See Fig 3b and S4 Fig). As seen in Fig 3c and Table 1, B2 shows maximum binding with KD value in the nano-molar range and the curves fit into a 1:1 binding model. C35 shows negligible binding and the rest of the constructs show binding lower than B2 with KD values in micro-molar range and the curves fit into a 2:1 binding model (See S5 Fig).

According to previous reports, FAK has to bind to both LD2 and LD4, failing which phosphorylation during signalling is reduced [8], which is observed in case of cancer [3], thus resulting in abnormal functioning of paxillin. We investigated this by analysing B2, which showed higher interaction than B1, despite missing the regulatory region of LD4 (Fig 1b). Similarly, C2 showed activity despite missing regulatory regions for both LD2 and LD4 and the presence of masking regions (similar activity observed in C1). This suggests that the masking region that is located between LD2 and LD4 is flexible to mask only a single LD motif but not both (Fig 3a). Interestingly, paxillin mutations associated with lung cancer were observed in the unstructured segments, particularly the regulatory region of LD2 and masking region of LD4 [3]. We hypothesize that these mutations prevent proper functioning of the regulatory regions, thus resulting in masking of either of the LD motifs causing abnormal functioning of paxillin. Evidence that these regions regulate FAT-paxillin binding was further provided in our study in the form of the bio-layer interferometry results; where C35 did not show any binding, but the constructs that included different lengths of the regulatory region along with the C35 region showed binding with KD values in the micro-molar range. This suggests that the LD2 region in these constructs is not masked, since it is seen in previous studies that the KD value for FAT binding to a single LD motif of paxillin is in micro-molar range. It also suggests that the region between residues 105–131 is sufficient for preventing the masking of LD2 region, thus allowing interaction with FAT (See illustrations in Fig 3b). Except B2 (that had a 1:1 binding stoichiometry and higher binding affinity), all other constructs (C35_1, C35_2, C35_3) showed a 2:1 binding stoichiometry. This suggests that both LD motifs of B2 engage both the FAT HP sites thus resulting in higher affinity; whereas in the other 3 constructs (C35_1, C35_2, C35_3), each FAT HP site (HP1 and HP2) interacts with individual molecules thus giving a 2:1 stoichiometry. This is in agreement with previous studies where both the LD motifs were found to interact with both HP1 and HP2 hydrophobic patches of FAT [16]. The higher affinity of B2 to FAT could be due to presence of both LD2 and LD4; the proposed intra-molecular regulatory regions could also play a role in the increased affinity. Therefore, we understand that the abnormal modulation in cancer involves redirection of FAK to a single LD motif; and targeting drugs for re-establishing the function at regulatory regions could be critical.

Unlike many existing techniques like array based yeast two hybrid assay, phage display method and tandem affinity purification; the strategy used here (combination of cell-free expression, filter based solubility assay and interaction study in HTP format) facilitated quick identification of the role of unstructured regions involved in paxillin-FAT interaction in HTP format. Particularly, in paxillin-FAK interactions, which determine focal adhesion and cellular signalling, we understood the structural masking and unmasking behaviour of unstructured segments in paxillin to determine FAK interaction. The structure of paxillin is not yet elucidated due to difficulties with respect to its disordered nature. In this study, the templates that we generated using the high throughput dissection strategy allowed us to analyze various regions of paxillin, with respect to structure, solubility and function. To our knowledge, this study is the first report of switch on and off mechanisms working together in controlling allosteric modulation/auto-inhibition in a human hub protein. As many eukaryotic proteins are disordered, our study opens avenues for analyzing novel modulations at allosteric sites using appropriate interaction studies, which could lead to identification of new drug target sites. In this regard, we hope the above strategy will be instrumental in understanding mechanisms of other disordered proteins as well, in days rather than months. This strategy could also be used as an initial screening method for techniques like SAXS, smFRET and others.

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Myc and Cancer Resistance

Curator: Larry H. Bernstein, MD, FCAP

 

Myc (c-Myc) is a regulator gene that codes for atranscription factor. The protein encoded by this gene is a multifunctional, nuclear phosphoprotein that plays a role in cell cycle progression, apoptosis and cellular transformation.[1]

Myc gene was first discovered in Burkitt lymphoma patients. In Burkitt lymphoma, cancer cells showchromosomal translocations, in which Chromosome 8 is frequently involved. Cloning the break-point of the fusion chromosomes revealed a gene that was similar to myelocytomatosis viral oncogene (v-Myc). Thus, the newfound cellular gene was named c-Myc.

http://www.ncbi.nlm.nih.gov/gene/17869

 

Protein increases signals that protect cancer cells

Researchers have identified a link between the expression of a cancer-related gene and cell-surface molecules that protect tumors from the immune system

http://med.stanford.edu/news/all-news/2016/03/protein-increases-signals-that-protect-cancer-cells.html

Depiction of the Myc protein

http://med.stanford.edu/news/all-news/2016/03/protein-increases-signals-that-protect-cancer-cells/_jcr_content/main/image.img.full.high.jpg

The Myc protein, depicted here, is mutated in more than half of all human cancers.   Petarg/Shutterstock

 

A cancer-associated protein called Myc directly controls the expression of two molecules known to protect tumor cells from the host’s immune system, according to a study by researchers at the Stanford University School of Medicine.

The finding is the first to link two critical steps in the development of a successful tumor: uncontrolled cell growth — when mutated or misregulated, Myc causes an increase in the levels of proteins that promote cell division — and an ability to outwit the immune molecules meant to stop it.

The study was published online March 10 inScience. Dean Felsher, MD, PhD, a professor of oncology and of pathology, is the senior author. The lead author is postdoctoral scholar Stephanie Casey, PhD. The work was conducted in collaboration with researchers at the University of Wurzburg.

“Our findings describe an intimate, causal connection between how oncogenes like Myc cause cancer and how those cancer cells manage to evade the immune system,” Felsher said.

‘Don’t eat me’ and ‘don’t find me’

One of the molecules is the CD47 protein, which researchers in the Stanford laboratory of Irving Weissman, MD, have discovered serves as a “don’t eat me” signal to ward off cancer-gobbling immune cells called macrophages. Weissman is the Virginia and D.K. Ludwig Professor for Clinical Investigation in Cancer Research and the director of Stanford’s Institute for Stem Cell Biology and Regenerative Medicine.

Nearly all human cancers express high levels of CD47 on their surfaces, and an antibody targeting the CD47 protein is currently in phase-1 clinical trials for a variety of human cancers.

The other molecule is a “don’t find me” protein called PD-L1, known to suppress the immune system during cancer and autoimmune diseases but also in normal pregnancy. It’s often overexpressed on human tumor cells. An antibody that binds to PD-L1 has been approved by the U.S. Food and Drug Administration to treat bladder and non-small-cell lung cancer, but it has been shown to be effective in the treatment of many cancers.

Dean Felsher

Programmed death-ligand 1 (PD-L1): an inhibitory immune pathway exploited by cancer

Image of PD-L1 binding to B7.1 and PD-1, deactivating T cell]

http://www.researchcancerimmunotherapy.com/images/pathways/pd-l1-hero.jpg

In cancer, Myc a usual suspect

Researchers in Felsher’s laboratory have been studying the Myc protein for more than a decade. It is encoded by a type of gene known as an oncogene. Oncogenes normally perform vital cellular functions, but when mutated or expressed incorrectly they become powerful cancer promoters. The Myc oncogene is mutated or misregulated in over half of all human cancers.

In particular, Felsher’s lab studies a phenomenon known as oncogene addiction, in which tumor cells are completely dependent on the expression of the oncogene. Blocking the expression of the Myc gene in these cases causes the complete regression of tumors in animals.

In 2010, Felsher and his colleagues showed that this regression could only occur in animals with an intact immune system, but it wasn’t clear why.

“Since then, I’ve had it in the back of my mind that there must be a relationship between Myc and the immune system,” said Felsher.

Turning off Myc expression

Casey and Felsher decided to see if there was a link between Myc expression and the levels of CD47 and PD-L1 proteins on the surface of cancer cells. To do so, they investigated what would happen if they actively turned off Myc expression in tumor cells from mice or humans. They found that a reduction in Myc caused a similar reduction in the levels of CD47 and PD-L1 proteins on the surface of mouse and human acute lymphoblastic leukemia cells, mouse and human liver cancer cells, human skin cancer cells, and human non-small-cell lung cancer cells. In contrast, levels of other immune regulatory molecules found on the surface of the cells were unaffected.

I’ve had it in the back of my mind that there must be a relationship between Myc and the immune system.

In publicly available gene expression data on tumor samples from hundreds of patients, they found that the levels of Myc expression correlated strongly with expression levels of CD47 and PD-L1 genes in liver, kidney and colorectal tumors.

The researchers then looked directly at the regulatory regions in the CD47 and PD-L1 genes. They found high levels of the Myc protein bound directly to the promoter regions of both CD47 and PD-L1 in mouse leukemia cells, as well as in a human bone cancer cell line. They were also able to verify that this binding increased the expression of the CD47 gene in a human blood cell line.

Possible treatment synergy

Finally, Casey and Felsher engineered mouse leukemia cells to constantly express CD47 or PD-L1 genes regardless of Myc expression status. These cells were better able than control cells to evade the detection of immune cells like macrophages and T cells, and, unlike in previous experiments from Felsher’s laboratory, tumors arising from these cells did not regress when Myc expression was deactivated.

“What we’re learning is that if CD47 and PD-L1 are present on the surfaces of cancer cells, even if you shut down a cancer gene, the animal doesn’t mount an adequate immune response, and the tumors don’t regress,” said Felsher.

The work suggests that a combination of therapies targeting the expression of both Myc and CD47 or PD-L1 could possibly have a synergistic effect by slowing or stopping tumor growth, and also waving a red flag at the immune system, Felsher said.

“There is a growing sense of tremendous excitement in the field of cancer immunotherapy,” said Felsher. “In many cases, it’s working. But it’s not been clear why some cancers are more sensitive than others. Our work highlights a direct link between oncogene expression and immune regulation that could be exploited to help patients.”

The research is an example of Stanford Medicine’s focus on precision health, the goal of which is to anticipate and prevent disease in the healthy and precisely diagnose and treat disease in the ill.

Other Stanford co-authors of the paper are oncology instructor Yulin Li, MD, PhD; postdoctoral scholars Ling Tong, PhD, Arvin Gouw, PhD, and Virginie Baylot, PhD; former research assistant Kelly Fitzgerald; and undergraduate student Rachel Do.

The research was supported by the National Institutes of Health (grants RO1CA089305, CA170378, CA184384, CA105102, P50 CA114747, U56CA112973, U01CA188383, 1F32CA177139 and 5T32AI07290).

 

The PD-L1 pathway downregulates cytotoxic T-cell activity to maintain immune homeostasis

Under normal conditions, the inhibitory ligands PD-L1 and PD-L2 play an important role in maintaining immune homeostasis.1 PD-L1 and PD-L2 bind to specific receptors on T cells. When bound to their receptors, cytotoxic T-cell activity is downregulated, thereby protecting normal cells from collateral damage.1,2

Image showing PD-L1 binding to B7.1 and PD-1 to deactivate T cells during immune response]

PD-L1

Broadly expressed in multiple tissue types, including hematopoietic, endothelial, and epithelial cells1,4

B7.1

Receptor expressed on activated T cells and dendritic cells3

PD-1

Receptor expressed primarily on activated T cells3

CONVERSELY, PD-L2 BINDS PRIMARILY TO PD-13

Image showing PD-L1 binding to B7.1 and PD-1 to deactivate T cells during immune response]

PD-L2

Restricted expression on immune cells and in some organs, such as the lung and colon1,4,5

PD-1

Receptor expressed primarily on activated T cells3

 

Many tumors can exploit the PD-L1 pathway to inhibit the antitumor response

In cancer, the PD-L1/B7.1 and PD-L1/PD-1 pathways can protect tumors from cytotoxic T cells, ultimately inhibiting the antitumor immune response in 2 ways.1-3

  • Deactivating cytotoxic T cells in the tumor microenvironment
  • Preventing priming and activation of new T cells in the lymph nodes and subsequent recruitment to the tumor

 

PD-L1 MAY INHIBIT CYTOTOXIC T-CELL ACTIVITY IN THE TUMOR MICROENVIRONMENT

Upregulation of PD-L1 can inhibit the last stages of the cancer immunity cycle by deactivating cytotoxic T cells in the tumor microenvironment.1

Activated T cells in the tumor microenvironment release interferon gamma.2

As a result, tumor cells and tumor-infiltrating immune cells overexpress PD-L1.2

PD-L1 binds to T-cell receptors B7.1 and PD-1, deactivating cytotoxic T cells. Once deactivated, T cells remain inhibited in the tumor microenvironment.1,2

PD-L1 MAY INHIBIT CANCER IMMUNITY CYCLE PROPAGATION IN THE LYMPH NODES

PD-L1 overexpression can also inhibit propagation of the cancer immunity cycle by preventing the priming and activation of T cells in the lymph nodes.1-3

PD-L1 expression is upregulated on dendritic cells within the tumor microenvironment.2,3

PD-L1–expressing dendritic cells travel from the tumor site to the lymph node.4

PD-L1 binds to B7.1 and PD-1 receptors on cytotoxic T cells, leading to their deactivation.3

http://www.researchcancerimmunotherapy.com/pathways/pd-l1-immune-evasion

 

The cancer immunity cycle characterizes the complex interactions between the immune system and cancer

The cancer immunity cycle describes a process of how one’s own immune system can protect the body against cancer. When performing optimally, the cycle is self-sustaining. With subsequent revolutions of the cycle, the breadth and depth of the immune response can be increased.1

 

STEPS 1-3: INITIATING AND PROPAGATING ANTICANCER IMMUNITY1

  • Oncogenesis leads to the expression of neoantigens that can be captured by dendritic cells
  • Dendritic cells can present antigens to T cells, priming and activating cytotoxic T cells to attack the cancer cells

STEPS 4-5: ACCESSING THE TUMOR1

  • Activated T cells travel to the tumor and infiltrate the tumor microenvironment

STEPS 6-7: CANCER-CELL RECOGNITION AND INITIATION OF CYTOTOXICITY1

  • Activated T cells can recognize and kill target cancer cells
  • Dying cancer cells release additional cancer antigens, propagating the cancer immunity cycle

 

 

 

Image of immunity cycle; explore Genentech cancer immunotherapy research on the cancer immunity cycle

http://www.researchcancerimmunotherapy.com/pathways/pd-l1

 

REFERENCES

  1. Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity. 2013;39:1-10. PMID: 23890059
  2. Chen DS, Irving BA, Hodi FS. Molecular pathways: next-generation immunotherapy—inhibiting programmed death-ligand 1 and programmed death-1. Clin Cancer Res. 2012;18:6580-6587. PMID: 23087408
  3. Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol. 2008;26:677-704. PMID: 18173375
  4. Motz GT, Coukos G. Deciphering and reversing tumor immune suppression. Immunity. 2013;39:61-73. PMID: 23890064

 

 

MYC regulates the antitumor immune response through CD47 and PD-L1

The clinical efficacy of monoclonal antibodies as cancer therapeutics is largely dependent upon their ability to target the tumor and induce a functional antitumor immune response. This two-step process of ADCC utilizes the response of innate immune cells to provide antitumor cytotoxicity triggered by the interaction of the Fc portion of the antibody with the Fc receptor on the immune cell. Immunotherapeutics that target NK cells, γδ T cells, macrophages and dendritic cells can, by augmenting the function of the immune response, enhance the antitumor activity of the antibodies. Advantages of such combination strategies include: the application to multiple existing antibodies (even across multiple diseases), the feasibility (from a regulatory perspective) of combining with previously approved agents and the assurance (to physicians and trial participants) that one of the ingredients – the antitumor antibody – has proven efficacy on its own. Here we discuss current strategies, including biologic rationale and clinical results, which enhance ADCC in the following ways: strategies that increase total target–monoclonal antibody–effector binding, strategies that trigger effector cell ‘activating’ signals and strategies that block effector cell ‘inhibitory’ signals.

Keywords: γδ T cells, ADCC, cancer, cytokines, IMiD, immunocytokines, immunomodulators, interleukins, monoclonal antibodies, NK cells, passive immunotherapy

Monoclonal antibodies (mAbs) can target tumor antigens on the surface of cancer cells and have a favorable toxicity profile in comparison with cytotoxic chemotherapy. Expression of tumor antigens is dynamic and inducible through agents such as Toll-like receptor (TLR) agonists, immunomodulatory drugs (IMiDs) and hypomethylating agents [1]. Following binding of the mAb to the tumor antigen, the Fc portion of the mAb interacts with the Fc receptor (FcR) on the surface of effector cells (i.e., NK cells, γδ T cells and macrophages), leading to antitumor cytotoxicity and/or phagocytosis of the tumor cell. FcR interactions can be stimulatory or inhibitory to the killer cell, depending on which FcR is triggered and on which cell. Stimulatory effects are mediated through FcγRI on macrophages, dendritic cells (DCs) and neutrophils, and FcγRIIIa on NK cells, DCs and macrophages. In murine models, the cytotoxicity resulting from FcR activation on a NK cell, γδ T cell and macrophage is responsible for antitumor activity [2]. The role of DCs should be noted: although not considered to be primary ADCC effector cells, they can respond to mAb-bound tumor cells via their own FcR-mediated activation and probably play a significant role in activating effector cells. Preclinical models have shown that, although not the effector cell, DCs are critical to the efficacy of mAb-mediated tumor elimination [3]. Equally, mAb-activated ADCC effector cells can induce DC activation [4] and the importance of this crosstalk is an increasing focus of study [5].

The antitumor effects of mAbs are caused by multiple mechanisms of action, including cell signaling agonism/antagonism, complement activation and ligand sequestration, although ADCC probably plays a predominant role in the efficacy of some mAbs. In a clinical series, a correlation between the affinity of the receptor FcγRIIIa (determined by inherited FcR polymorphisms) and the clinical response to mAb therapy, supporting the significance of the innate immune response [610]. Several strategies could potentially improve the innate response following FcR activation by a mAb (Figure 1):

Quantitatively increasing the density of the bound target, mAb or the effector cells;

Stimulation of the effector cell by targeting the NK cell, γδ T cell and/or macrophage with small molecules, cytokines or agonistic antibodies;

Blocking an inhibitory interaction between the NK cell or macrophage and the tumor cell.

 

An external file that holds a picture, illustration, etc. Object name is nihms384451f1.jpg

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3386352/bin/nihms384451f1.jpg

Enhancing ADCC

FcR: Fc receptor; HDACi: Histone deacetylase inhibitor; IMiD: Immunomodulator; KIR: Killer immunoglobulin-like receptor;

The ability of the combination approaches to enhance ADCC is largely determined by the capacity of the mAb to induce ADCC. Since the approval of the first mAb for the treatment of non-Hodgkin’s lymphoma, rituximab (RTX), in 1997, several mAbs have become standard of care for the treatment of both solid tumors and hematologic malignancies, including trastuzumab (TRAST), alemtuzumab, cetuximab, panitumumab and ofatumumab [11]. As noted above, clinical series among lymphoma patients treated with an anti-CD20 mAb (RTX) [6,7], HER2-expressing breast cancer receiving anti-HER2 mAb therapy (TRAST) [8] or colorectal cancer patients treated with an anti-EGFR mAb (cetuximab) [9,10] observed a correlation between clinical benefit and FcγRIIIa genotype, with patients who have higher-affinity polymorphisms demonstrating superior clinical outcomes. By contrast, the anti-EGFR mAb panitumumab does not induce ADCC, owing to a different Fc isotype that does not bind to the FcγRIIIa. Therefore, when considering enhancement of ADCC, such approaches are limited to combinations with mAbs that activate the FcR. Nonetheless, an advantage of this dual therapy strategy is that mAbs yet to be discovered against currently unknown tumor antigens may be combined with the therapeutics discussed herein.

Increasing target–mAb–effector binding

As the central element in the target–mAb–effector cell unit, the mAb seems to be a probable candidate for improvements, either in its antigen-binding or its Fc-binding domains. This approach has been heavily pursued with some degree of success [1215]. Antibody engineering to improve interaction between the target or FcR requires that each new antibody be individually developed and tested as a new entity.

Increasing the antigen target

Tumor cells with a lower density of antigen targets are less responsive to mAbs than higher antigen-expressing diseases [16]. Therefore, it seems logical to try to increase the expression of the target on tumor cells. Antigen expression can be upregulated by cytokines [17], ionizing radiation [18], natural metabolites [19] and hypomethylating agents such as decitabine [20]. In addition, the family of TLR9 agonists known as CpG oligodeoxynucleotides (CpG ODN) can induce CD20 expression on malignant B cells [2123]. Taken together with data showing the activating effect of CpG ODN on effector cells (discussed below), it seems reasonable that the combination of CpG ODN with mAb might have synergistic efficacy. Clinical series, however, have tested CpG ODN administered intravenously or subcutaneously and have observed little efficacy in Phase I and II studies [2426] in low-grade lymphoma. One possible limitation of these studies has been their application to diseases (primarily follicular and mantle cell lymphoma) known to already have high expression of the relevant antigen (CD20). It is plausible that increasing antigen expression on low antigen-expressing diseases such as chronic lymphocytic leukemia could have a greater increase in relative efficacy. To this end, monotherapy studies have recently been undertaken [27,301] and should lead to combination trials.

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Effector cells: γδ T cells

The role of NK cells and macrophages in mediating ADCC has been well established; however, only recently have γδ T cells been found to play a role as ADCC effectors. Typically, this population is considered as a minor subset (<5% of circulating T cells), although they may infiltrate tumors of epithelial origin preferentially and constitute a large portion of the tumor-infiltrating lymphocytes in cancers such as breast carcinoma. The combination of HLA-unrestricted cytotoxicity against multiple tumor cell lines of various histologies, secretion of cytolytic granules and proinflammatory cytokines such as TNF-α, IL-17 and IFN-γ make γδ T cells potentially potent antitumor effectors [32,33].

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TLR agonists    

In addition to its aforementioned induction of CD20, CpG ODN also indirectly augments innate immune function. TLRs are specialized to recognize pathogen-associated molecular patterns; they stimulate plasmacytoid DCs and B cells [53], and one of many plasmacytoid DC responses to stimulation by CpG ODNs is activation of local NK cells, thus improving spontaneous cytotoxicity and ADCC [54]. CpG ODN effects on NK cells appeared to be indirect and IFN-γ production by T cells (possibly in response to plasmacytoid DC activation) has been hypothesized as the intermediary of NK cell activation.

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Immunomodulatory drugs

IMiDs have shown clinical activity in multiple hematologic malignancies despite their primary mechanism of action being unclear. Among their biologic effects (particularly lenalidomide) there are demonstrable and pleiotropic effects on immune cells and signaling molecules. These include enhancement of in vitro NK cell- and monocyte-mediated ADCC on RTX-coated [68] as well as TRAST- and cetuximab-coated tumor cells [69]. In vivo studies in a human lymphoma severe combined immune deficiency mouse model demonstrated significant increases in NK cell recruitment to tumors mediated via microenvironment cytokine changes and augmented RTX-associated ADCC [70]. Studies suggest that IMiD activation of NK cells occurs indirectly; partly via IL-2 induction by T cells [71]. Clinically, a recent study noted significant increases in peripheral blood NK cells, NK cell cytotoxicity and serum IL-2, IL-15 and GM-CSF [72], the potential ADCC-promoting effects of which are discussed below.

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PD-1

PD-1 is a negative regulatory member of the CD28 superfamily expressed on the surface of activated T cells, B cells, NK cells and macrophages, similar to but more broadly regulatory than CTLA-4. Its two known ligands, PD-L1 and PD-L2, are both expressed on a variety of tumor cell lines. The PD-1–PD-L1 axis modulates the NK cell versus multiple myeloma effect, as seen by its blockade enhancing NK cell function against autologous primary myeloma cells, seemingly through effects on NK cell trafficking, immune complex formation with myeloma cells and cytotoxicity specifically toward PD-L1(+) tumor cells [179]. Two anti-PD-1 mAbs (BMS-936558 and CT-011) are currently in clinical trials, the latter in a combination study with RTX for patients with low-grade follicular lymphoma [314].

ConclusionThe recent approval of an anti-CTLA4 mAb has demonstrated that modulating the immune response can improve patient survival [180,181]. As the immune response is a major determinant of mAb efficacy, the opportunity now exists to combine mAb therapy with IMiDs to enhance their antitumor efficacy. Remarkable advances in the basic science of cellular immunology have increased our understanding of the effector mechanisms of mAb antitumor efficacy. Whereas the earliest iterations of such combinations, for example IL-2 and GM-CSF, may have augmented both effector and suppressive cells, newer approaches such as IL-15 and TLR agonists may more efficiently activate effector cells while minimizing the influence of suppressive cells. Despite these encouraging rationale and preliminary data, clinical evidence is still required to demonstrate whether combination therapies will increase the antitumor effects of mAb.

Still, this approach is unique in combining a tumor-targeting therapy, the mAb, with an immune-enhancing therapy. If successful, these therapies may be combined with multiple mAbs in routine practice, as well as novel mAbs yet to be developed. Various approaches including augmenting antigen expression, stimulating the innate response and blocking inhibitory signals are being explored to determine the optimal synergy with mAb therapies. Therapies targeting NK cells, γδ T cells, macrophages and DCs may ultimately be used in combination to further augment ADCC. Encouraging preclinical studies have led to a number of promising therapeutics, and the results of proof-of-concept clinical trials are eagerly awaited.

PD-L1, other targeted therapies await more standardized IHC

February 2016—Immunohistochemistry is heading down a path toward more standardization, and that’s essential as it plays an increasing role in rapidly expanding immunotherapy, says David L. Rimm, MD, PhD, professor of pathology and of medicine (oncology) and director of translational pathology at Yale University School of Medicine. As a co-presenter of a webinar produced by CAP TODAY in collaboration with Horizon Diagnostics, titled “Immunohistochemistry Through the Lens of Companion Diagnostics” (http://j.mp/ihclens_webinar), he analyzes the core challenges of IHC’s adaptation to the needs of precision medicine: binary versus continuous IHC, measuring as opposed to counting or viewing by the pathologist, automation, and assay performance versus protein measurement.

“Immunohistochemistry is 99 percent binary already,” Dr. Rimm points out. “There are only a few assays in our labs—ER, PR, HER2, Ki-67, and maybe a few more—where we really are looking at a continuous curve or a level of expression.”

Two criteria in the 2010 ASCO/CAP guidelines on ER and PR testing in breast cancer patients are key, he says: 1) the percentage of cells staining and 2) any immunoreactivity. “The first is hard to estimate, but the guidelines recommend the use of greater than or equal to one percent of cells that are immunoreactive. That means they could have a tiny bit of signal or they could have a huge amount of signal and they would be considered immunoreactive, which thereby makes this a binary test.”

Having the test be binary can be a problem for companion diagnostic purposes because any immunoreactivity is dependent on the laboratory threshold and counterstain. For example, if two of the same spots, serial sections on a tissue microarray, were shown side by side, one with and one without the hematoxylin counterstain, “you might see the counterstain make this positive test into a negative by eye, which is a potential problem with IHC when you have a binary stain.” (Fig. 1).

Fig1

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Dr. Rimm describes a small study done with three different CLIA-certified labs, each using a different FDA-approved antibody and measuring about 500 breast cancer cases on a tissue microarray. The study showed there can be fairly significant discordance between labs—between 18 and 30 percent discordance—in terms of the cases that were positive. “In fact, if we look at outcome, 18 percent of the cases were called positive in Lab Two but were negative in Lab Three. Lab Three showed outcomes similar to the double positives whereas Lab Two had false-negatives.” This is an important problem that occurs when we try to binarize our immunohistochemistry, he says.

Counting is more variable in a real-world setting due to the variability of the threshold for considering a case positive. “You can easily calculate that if your threshold was five percent, then you’d have 70 percent positive cells. And you would easily call this positive. But if you added more hematoxylin because that’s how your pathologist liked it, then perhaps you’d only have 30 percent positive. So this is the risk of using thresholds.” (Fig. 2).

Fig2

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Although this is done in all of immunohistochemistry today, Dr. Rimm thinks it is an important consideration as IHC transitions to more standardized form. “An H score—intensity times area, which has been attempted many times, can’t be done by human beings. Pathologists try but have failed.”

“We can’t do those intensities by eye. We have to measure them with a machine. But we get a very different piece of information content when we measure intensity, as opposed to measuring the percentage of cells above a threshold. In sum, more information is present in a measurement than in counting.”

Pathologists read slides for a living, so it’s uncomfortable to think about giving that up in order to use a machine to measure the slides. “But I think if we want to serve our clients and our patients, we really owe them the accuracy of the 21st century as opposed to the methods of the 20th century.” (Fig. 3).

A shows comparison of a quantitative fluorescence score on the x axis versus an H-score on the y axis. Note the noncontinuous nature of human estimation of intensity times area (H-score). B) The survival curve in a population of lung cancer cases using the H-score. C) The survival curve in the same population using the quantitative score. (Source: David Rimm, MD, PhD)

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A shows comparison of a quantitative fluorescence score on the x axis versus an H-score on the y axis. Note the noncontinuous nature of human estimation of intensity times area (H-score). B) The survival curve in a population of lung cancer cases using the H-score. C) The survival curve in the same population using the quantitative score. (Source: David Rimm, MD, PhD)

Among the currently available quantitative measuring devices are the Visiopharm, VIAS (Ventana), Aperio (Leica), InForm (Perkin-Elmer), and Definiens platforms. “We use the platform invented in my lab, called Aqua [Automated Quantitative Analysis], but this is now owned by Genoptix/Novartis. Genoptix intends to provide commercial tests using Aqua internally,” Dr. Rimm says, “as well as enable platform and commercial testing through partnership with additional reference lab providers.

“There are many quantification platforms,” he adds, “and I believe that any of them, used properly, can be effective in measurement.”

(Of the 265 participants in the CAP PM2 Survey, 2015 B mailing, who reported using an imaging system for quantification, 4.6 percent use VIAS, 4.1 percent use ACIS, 0.8 use Applied Imaging, and 10 percent use “other” imaging systems. Of the 1,359 Survey participants who responded to the question about use of an imaging system to analyze hormone receptor slides, 1,094, or 80.5 percent, reported not using any imaging system for quantification.)

Says Dr. Rimm: “The first platform we used to try to quantitate some DAB stain slides was actually the Aperio Nuclear Image Analysis algorithm. But the problem with DAB is that you can’t see through it. And so inherently it’s physically flawed as a method for accurate measurement.” He compares DAB to looking at stacks of pennies from above, where their height and quantity can’t be surmised, as opposed to from the side, where their numbers can be accurately estimated. “This is why I don’t use, in general, DAB-type technologies or any chromogen.”

Fluorescence doesn’t have this problem, and that is the reason Dr. Rimm began using fluorescence as a quantitative method. “We try to be entirely quantitative without any feature extraction. So we define epithelial tumors using a mask of cytokeratin. We define a mask by bleeding and dilating, filling some holes, and then ultimately measure the intensity of each cell, or of each target we’re looking for. In this case, in a molecularly defined compartment.”

Compartments can be defined by any type of molecular interactions. “We defined DAPI-positive pixels as nuclei, and we measure the intensity of the estrogen receptor within the compartment. And that gives us an intensity over an area or the equivalent of a concentration.” Many other fluorescent tools can be used in this same manner, but he cautions against use of fluorescent tools that group and count. “That’s a second approach that can be used, but the result gives you a count instead of a measurement.”

When comparing a pathologist’s reading versus a quantitative immunofluorescence score, he notes, pathologists actually don’t generate a continuous score. Instead, pathologists tend to use groups. “We tend to use a 100 or a 200 or an even number. We never say, ‘Well, it’s 37 percent positive.’ We say, ‘It’s 40 percent positive,’ because we know we can’t reproducibly tell 37 from 38 from 40 percent positive.”

The result of that is a noncontinuous scoring result, which doesn’t give the information content of quantitative measurement. A comparison between the two methods shows that at times, where quantitative measurement shows a significant difference in outcome, nonquantitative measure or an H-score difference may not show a difference in outcome. (Fig. 3 illustrates this concept.)

“Pathologists tend to group things, and we also tend to overestimate. It’s not that pathologists are bad readers. It’s just the tendency of the human eye because of our ability to distinguish different intensities and the subtle difference between intensities. But even if you compare two quantitative methods, you can see that the method where light absorbance occurs—that is the percent positive nuclei by Aperio, which is a chromogen-based method—tends to saturate. This is, in fact, amplified dramatically when you look at something with a wide dynamic range like HER2.” (Fig. 4).

Fig4

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In one study, researchers found less than one percent discordance—essentially no discordance—between two antibodies (Dekker TJ, et al. Breast Cancer Res. 2012;14[3]:R93). But looking at these results graphed quantitatively, you would see a very different result, Dr. Rimm says. “You can see a whole group of cases down below where there’s very low extracellular domain and very high cytoplasmic domain. In fact, some of these cases have essentially no extracellular domain, but high levels of cytoplasmic domain, and other cases have roughly equal levels of each” (Carvajal-Hausdorf DE, et al. J Natl Cancer Inst.2015;107[8]:pii:djv136).

Recent studies by Dr. Rimm’s group have shown this to have clinical implications. He looked at patients treated with trastuzumab in the absence of chemotherapy, in an unusual study called the HeCOG (Hellenic Cooperative Oncology Group) trial.

“We found that patients who had high levels of both extracellular and intracellular domain have much more benefit than patients who are missing the extracellular domain and thereby missing the trastuzumab binding site.” Follow-up studies are being done to validate this finding in larger cohorts.

Preanalytical variables, Dr. Rimm emphasizes, can have significant effects on IHC results, and more than 175 of them have been identified. “These are basically all the things we can’t control, which is the ultimate argument for standardization.”

In a surprising study by Flory Nkoy, et al., he says, it was shown that breast cancer specimens were more likely to be ER negative if the patient’s surgery was on a Friday because there was a higher ER-negative rate on Friday than on Monday. “So how could that be? Well, it was clearly the fact that the tissue was sitting over the weekend. And when it sat over the weekend, the ER positivity rate was going down” (Arch Pathol Lab Med. 2010;134:606–612).

Another study showed that after one hour, four hours, and eight hours of storage at room temperature, you lose significant amounts of staining, Dr. Rimm says. “And perhaps the best nonquantitative study or H-score-based study of this phenomenon was done by Isil Yildiz-Aktas, et al., where a significant decrease in the estrogen receptor score was found after only three hours in delay to fixation” (Mod Pathol. 2012;25:1098–1105).

How long the slide is left to sit after it is cut is another preanalytical variable to be concerned with. “In the clinical lab, that’s not often a problem since we cut them, then stain them right away. But in a research setting, a fresh-cut slide can look very different from a slide that’s two days old, six days old, or 30 days old, where a 2+ spot on a breast cancer patient becomes negative after 30 days sitting on a lab bench. So those are both key variables to be mindful of.”

One solution for those preanalytic variables is trying to prevent delayed time to fixation. “And probably time to fixation is one of the main preanalytic variables, although it’s only one of the many hundreds of variables. The method we use to try to get around this problem is to use core biopsies or allow rapid and complete fixation, and then other things can be done.”

Finally, he warns, don’t cut your tissue until right before you stain it. “If you’re asked to send a tissue out to a collaborator or someone who is going to use it for research purposes later, we recommend coring and re-embedding the core, or sending the whole block. Unstained sections, when not properly stored in a vacuum, will ultimately be damaged by hydration or oxidation, both of which lead to loss of antigenicity.”

The crux of the matter is assay performance versus protein measurement, Dr. Rimm says. “In the last six to nine months, we really are faced with this problem in spades, as PD-L1 has become a very important companion diagnostic.”

There are now four PD-L1 drugs with complementary or companion diagnostic tests (Fig. 5). One of the FDA-approved drugs, nivolumab (Opdivo, Bristol-Myers Squibb), for example, uses a clone called 28-8, which is provided by Dako in an assay, a complementary diagnostic assay, and with the following suggested scoring system: one percent, five percent, or 10 percent. In contrast, pembrolizumab (Keytruda, Merck) is also now FDA-approved but requires a companion diagnostic test that uses a different antibody, although the same Dako Link 48 platform. This diagnostic has a different scoring system of less than one percent, one to 49 percent, and 50 percent and over.

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Two other companies, Roche/Genentech and AstraZeneca, also have drugs in trials that may or may not have companion diagnostic testing, though both have already identified a partner and a unique antibody (neither of those listed above) and companion diagnostic testing scores used in their clinical trials.

“So what’s a pathologist to do?” Dr. Rimm says. “Well, there are a few problems with this. First of all, what we really should be doing is measuring PD-L1. That’s the target and that’s what should ultimately predict response. But instead what we’re stuck with, through the intricacies of the way our field has grown and our legacy, is closed-system assays. While these probably do measure PD-L1, we do not know how these compare to each other.” Two parallel large multi-institutional studies are addressing this issue now, he says.

There are solutions for managing these closed-system assays to be sure the assay is working in your lab and that you can get the right answer, Dr. Rimm says. His laboratory uses a closed-system assay for PD-L1, relying not on the defined system but rather on a test system it has developed in doing a study with different investigators.

Sample runs by these different investigators show the potentially high variability, he says. “In a scan of results, no one would deny which spots are the positive spots and which are the negative.” But the difference in staining prevents accurate measurement of these things and shows the variability inherent even in a closed-box system.

A comparison of two closed-box systems, the SP1 run on the Discovery Ultra on Ventana, and the SP1, same antibody, run on the Dako closed-box system, also shows that, in fact, there’s not 100 percent agreement using same-day, same-FDA-cleared antibody staining and different autostainers. So automation may not solve the problem, Dr. Rimm notes (Fig. 6).

Fig6

“When running these in a quantitative fashion and measuring them quantitatively, there are actually differences in the way these closed-box systems run. And so you, as the pathologist, have to be the one who makes sure your assays are correct, your thresholds are correct, and your measurements are accurate.”

The way to do that, he believes, is to use standardization or index arrays. An index array of HER2 that his laboratory developed has 3+ amplified, 2+ amplified, not amplified, and so on from 80 cases in the lab’s archive, shown stained with immunofluorescence and quantitative and DAB stain. “It was only with this standardization array, run every time we ran our stainer, that we were able to draw the conclusions in the previous study about extracellular versus cytoplasmic domain.”

Companies have realized the importance of this, and specifically companies like NantOmics (formerly OncoPlexDx) have realized they can exactly quantitate the amount of tissue on a slide using a specialized mass spectrometry method, he says. “They can actually give you amol/µg of total protein.”

He and colleagues are working with NantOmics now to try to convert from amols to protein to average quantitative fluorescent scores to help build these standards and make standard arrays more accurate. “This is still a work in progress, but I believe this is ultimately the kind of accuracy that can standardize all of our labs. We have shown that the quantitative fluorescence system is truly linear and quantitative for EGFR measurements when using mass spectrometry as a gold standard.” They are preparing to submit a manuscript with this data.

In the interim, Dr. Rimm’s laboratory has begun working also with Horizon Diagnostics, employing Horizon’s experimental 15-spot positive-control array. “When you use this array and quantitate it with quantitative fluorescence, you get a very interesting profile. If a cut point is set at one point, you would see three clearly positive cells or spots and 12 clearly negative spots with two different antibodies. But is that the threshold?”

“In fact, using a little higher score and a very quantitative test, you might find that the threshold may, in fact, be a little bit lower than that.” It turns out that only three of these 12 spots are true negatives. The others at least have some level of RNA, and some have a lot. “So how do we handle these? And are these behaving the same way with multiple antibodies?” Parallel results, finding nearly the same threshold case, have been found using SP142 from Ventana, E1L3N from Cell Signaling, and SP263 from Ventana.

Studies to address those issues are still in the early stage, he says. He cautions that there is variance in these assays, and more work is being done to reproduce the data. “But I think the important point is that, using these kinds of arrays, you can definitively determine whether your lab has the same cut point as every other lab. And were we to quantitate this with mass spectrometry, we would know exactly the break point for use in the future.”

Dr. Rimm’s laboratory has also built its own PD-L1 index tissue microarray with a number of its own tumor slides ranging from very low to very high expressors, a series of cell lines, and including some placenta-positive controls on normal tumor. He has found that generating an index array has advantages, and he encourages other laboratories to prepare their own index arrays to increase the accuracy and reproducibility of their laboratory-developed tests. “You can produce these in your own lab so that you can be sure you can standardize your tests run in your clinical lab from day to day and week to week as part of an LDT.”

“If we think about it, there really are no clinical antibodies today that are truly quantitative,” Dr. Rimm says. “And when there are, new protocols will be required, but I believe those protocols are now in existence. We just await the clinical trials that require truly quantitative protein measurement or in situ proteomics.”

In that process of moving toward in situ proteomics, suggests web-inar co-presenter Clive Taylor, MD, DPhil, professor of pathology in the Keck School of Medicine at the University of Southern California, FDA approval, per se, will not solve any of the problems discussed in the webinar. (See the January 2016 issue for the full report of Dr. Taylor’s presentation.) “I think what the FDA approval will do is demand that we find solutions to these problems ourselves. The FDA’s attitude is, to a large degree, dependent on the claim. So if we just use immunohistochemistry as a simple stain, then the FDA classes that as sort of class I, level 1. And we can do that [IHC stain] without having to get preapproval by the FDA.

“On the other hand, if we take something like the well-established HercepTest, where based on the result of that test alone, it’s decided whether or not the patient gets treatment, treatment that’s very expensive and treatment that has benefits and…side effects. That claim is, in fact, a very high-level claim. And for that, the FDA is demanding high-level data, which I think is entirely appropriate,” Dr. Taylor says.

Most of these upcoming companion diagnostics, if not all, he says, will be regarded by the FDA as class III, high level or high complexity. They will require a premarket approval study in conjunction with a clinical trial. And the FDA will demand high standards of control and performance, eventually. “There are not many labs that can produce those high standards as in-house or lab-developed tests today. And even the companies currently in trials are not producing the improved performance level for these tests that we are talking about today, as being required for high-quality quantitative and reproducible companion diagnostics. Eventually, I am convinced we will have to do that. It’s just that it will take time to get there.”

The FDA can only approve what is brought to it, Dr. Rimm points out. And so a true, fully quantitative IHC-based assay has presumably never been submitted, or at least never been approved by the FDA. “What we’re seeing instead are the assays that the FDA has approved, which are well defined and rigorously submitted. However, the result is a closed system that we use, which may or may not accurately measure PD-L1 on the slide, depending upon preanalytic variables and individual laboratories’ methods.”

“So questions keep popping up. And I can only say that we, as pathologists, have the final responsibility to our patients. And while it may not be recommended and it may change in the future, right now lab-derived tests or LDTs may be more accurate than FDA-approved platforms.”

“If you think about it, in molecular diagnostics where I’m familiar with EFGR and BRAF and KRAS tests, in that testing setting, less than 25 percent of the labs that do that test actually use the FDA-approved test,” Dr. Rimm says. “The remainder of the labs do their own LDTs, including our labs here at Yale.”

It wouldn’t surprise him if the same thing happens for PD-L1. “I’m aware of at least two labs—and we probably will be the third—that devise our own LDT for PD-L1 testing using the standards I’ve discussed, using array-type controls to be sure that our levels are correct, and then using a scoring system that we derived.”

“We aren’t really in a position to know at the time that we receive a piece of lung cancer tissue whether the oncologist is going to use pembrolizumab, which requires a companion diagnostic, or nivolumab, or the other drugs, which may or may not require a companion diagnostic. So in that sense, we’re almost bound to use an LDT,” Dr. Rimm says, since his lab can’t actually run four different potentially incongruent, though FDA-approved, tests for PD-L1.

Until a truly quantitative approach is developed and submitted to the FDA and approved, Dr. Taylor believes we won’t see things changing. “The algorithms that currently are approved have been approved on the basis that they can produce a similar result to a consensus group of pathologists. So they’re only as good as the pathologists.”

“As Dr. Rimm has discussed, I actually believe we can get a much better result than the pathologists can get with their naked eye. We have to get away from comparing it to what we currently can do and start to try to construct a proper test, just like we did in the clinical lab 30 years ago when we automated the clinical lab,” Dr. Taylor says. “We need to automate anatomic pathology, including the sample preparation, the assay process, and the reading, all three together in a closed system. And we’re nibbling away at the edges of it. We’ll get there, but it’ll take some time.”

Dr. Rimm is skeptical that the diagnostics field has learned any lessons from HercepTest and the companion diagnostics world of almost 20 years ago. “The submissions to the FDA for PD-L1 look very similar to what was submitted in 1998 for the HercepTest, the companion diagnostic test for trastuzumab [Herceptin]. And that’s disappointing. I think that is 20-year-old technology and we can do better. But even if we want to use the 20- or 40-year-old DAB-based technology, we should still be standardizing it and having a mechanism for standardization and having defined thresholds.”

As future FDA submissions come in, Dr. Rimm hopes that “even if they’re not quantitated, they can be standardized as to where the thresholds occur, so that we can be sure we deliver the best possible care to patients. And in the interim, I think we, as pathologists, will have to do that standardization with an LDT to be sure we’re giving our best results.”

Dr. Taylor warns that there is only a limited number of labs in the country and in the world that will be able to produce these LDTs, because of the complexity. “The FDA has already said in a position paper that it believes it may have to regulate LDTs to some extent. And what that will mean is that in the validation process, your own LDT will start to approach what is required for an FDA-approved test. And most labs are in no position to be able to do that.”

“So I think we’re going to come to a blending here, all forced by companion diagnostics. This is in situ proteomics,” Dr. Taylor says. “It’s a new test, essentially. It’s not straightforward immunohistochemistry, but a new test. And I think the fluorescence approach that Dr. Rimm has used has a lot of advantages in relating signal to target in terms of figure out what the best test is and stop comparing it to the pathologists. We should compare it to the best assay we can produce.”

With respect to the PD-L1 problem, Dr. Rimm notes, “I would point out that there is a so-called ‘Blueprint’ for comparison of the different antibodies and the different FDA assays, or potentially FDA-submitted tests anyway, to see how equivalent they are.” Similarly, he adds, the National Comprehensive Cancer Network recently issued a press release describing a multi-institutional study to assess the FDA-approved assay but also including an LDT (the Cell Signaling antibody E1L3N using the Leica Bond staining platform).

He points to a newly published study by his group (McLaughlin J, et al. JAMA Oncol. 2016;2[1]:46–54), finding that objective determination of PD-L1 protein levels in non-small cell lung cancer reveals heterogeneity within tumors and prominent interassay variability or discordance. The authors concluded that future studies measuring PD-L1 quantitatively in patients treated with anti-PD-1 and anti PD-L1 therapies may better address the prognostic or predictive value of these biomarkers. With future rigorous studies, including tissues with known responses to anti-PD-1 and anti-PD-L1 therapies, researchers could determine the optimal assay, PD-L1 antibody, and the best cut point for PD-L1 positivity.

Other work that will probably come out in mid-2016 from Dr. Rimm’s group has shown that expression of PD-L1 is largely bimodal, he says. “That is, there’s a group of patients that express a lot, and then there’s another group of patients that expresses a little or none.”

So time will tell how PD-L1 will be scored. “But if you look at the data from the Merck study and their cut point of greater than 50 percent, or even the cut point from the AstraZeneca studies of greater than 25 percent, you’re really dichotomizing the population into patients who are truly PD-LI positive from patients who are negative or almost negative.”

“Of course, we don’t want to miss patients in that negative to almost-negative group who will respond,” Dr. Rimm says. “On the other hand, we probably will have fairly good specificity and sensitivity with the assay defined by Merck and Dako with 22C3 as was recently published” (Robert C, et al. N Engl J Med. 2015;372[26]:2521–2532).

Many difficulties lie ahead, as researchers try to weigh the merits of different drugs with different approved tests on different platforms, involving different antibodies, Dr. Taylor says. “Does the lab try to set up four different PD-L1s, and if we only have one platform and not another, what do we do about that?” He thinks the tests may often be sent out to larger reference labs or academic centers as a result.

Dr. Rimm confirms that his own lab’s LDT—although literally thousands of PD-L1 tests have been conducted using it—is not yet up and running in the Yale CLIA laboratory, and in the meantime the IHC slides are being sent out to a commercial vendor.

Eventually, Dr. Taylor believes, the pressure of these dilemmas will lead the diagnostics field to develop an immunoassay on tissue sections. “We’ve never been forced to do that before, but once we are, that will produce a huge change in diagnostic capability and research capability.”

Anti–PD-1/PD-L1 therapy of human cancer: past, present, and future

Lieping Chen and  http://www.jci.org/articles/view/80011

The cDNA of programmed cell death 1 (PD-1) was isolated in 1992 from a murine T cell hybridoma and a hematopoietic progenitor cell line undergoing apoptosis (1). Genetic ablation studies showed that deficiencies in PD-1 resulted in different autoimmune phenotypes in various mouse strains (2, 3). PD-1–deficient allogeneic T cells with transgenic T cell receptors exhibited augmented responses to alloantigens, indicating that the PD-1 on T cells plays a negative regulatory role in response to antigen (2).

Several studies contributed to the discovery of the molecules that interact with PD-1. In 1999, the B7 homolog 1 (B7-H1, also called programmed death ligand-1 [PD-L1]) was identified independently from PD-1 using molecular cloning and human expressed-sequence tag database searches based on its homology with B7 family molecules, and it was shown that PD-L1 acts as an inhibitor of human T cell responses in vitro (4). These two independent lines of study merged one year later when Freeman, Wood, and Honjo’s laboratories showed that PD-L1 is a binding and functional partner of PD-1 (5). Next, it was determined that PD-L1–deficient mice (Pdl1 KO mice) were prone to autoimmune diseases, although this strain of mice did not spontaneously develop such diseases (6). It became clear later that the PD-L1/PD-1 interaction plays a dominant role in the suppression of T cell responses in vivo, especially in the tumor microenvironment (7, 8).

In addition to PD-L1, another PD-1 ligand called B7-DC (also known as PD-L2) was also identified by the laboratories of Pardoll (9) and Freeman (10). This PD-1 ligand was found to be selectively expressed on DCs and delivered its suppressive signal by binding PD-1. Mutagenesis studies of PD-L1 and PD-L2 molecules guided by molecular modeling revealed that both PD-L1 and PD-L2 could interact with other molecules in addition to PD-1 and suggested that these interactions had distinct functions (11). The functional predictions from these mutagenesis studies were later confirmed when PD-L1 was found to interact with CD80 on activated T cells to mediate an inhibitory signal (12, 13). This finding came as a surprise because CD80 had been previously identified as a functional ligand for CD28 and cytotoxic T lymphocyte antigen-4 (CTLA-4) (14, 15). PD-L2 was also found to interact with repulsive guidance molecule family member b (RGMb), a molecule that is highly enriched in lung macrophages and may be required for induction of respiratory tolerance (16). With at least five interacting molecules in the PD-1/PD-L1 pathway (referred to as the PD pathway) (Figure 1), further studies will be required to understand the relative contributions of these molecules during activation or suppression of T cells.

The PD pathway. The PD pathway has at least 5 interacting molecules. PD-...

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The PD pathway.

The PD pathway has at least 5 interacting molecules. PD-L1 and PD-L2, with different expression patterns, were identified as ligands of PD-1, and the interaction of PD-L1 or PD-L2 with PD-1 may induce T cell suppression. PD-L1 was found to interact with B7-1 (CD80) on activated T cells and inhibit T cell activity. PD-L2 has a second receptor, RGMb; initially, this interaction activates T cells, but it subsequently induces respiratory tolerance. PD-L1 on tumor cells can also act as a receptor, and the signal delivered from PD-1 on T cells can protect tumor cells from cytotoxic lysis.

The discovery of the PD pathway did not automatically justify its application to cancer therapy, especially after the initial PD-1–deficient mouse studies, which suggested that PD-1 deficiency increases the incidence of autoimmune diseases (2, 3). In our initial work to characterize PD-L1 and its function, PDL1 mRNA was found to be broadly expressed in various tissues (17). However, normal human tissues seldom express PD-L1 protein on their cell surface, with the exception of tonsil (17), placenta (18), and a small fraction of macrophage-like cells in lung and liver (17), suggesting that, under normal physiological conditions, PDL1 mRNA is under tight posttranscriptional regulation. In sharp contrast, PD-L1 protein is abundantly expressed on the cell surface in various human cancers, as indicated by immunohistochemistry in frozen human tumor sections. Additionally, the pattern of PD-L1 expression was found to be focal rather than diffuse in most human cancers (17). In fact, the majority of in vitro–cultured tumor lines of both human and mouse origin are PD-L1–negative on the cell surface, despite overwhelming PD-L1 signal in specimens that are freshly isolated from patients with cancer (17, 19). This discrepancy was explained by the finding that IFN-γ upregulates PD-L1 on the cell surface of normal tissues and in various tumor lines (7, 17, 19). It was widely thought that IFN-γ typically promotes, rather than suppresses, T cell responses by stimulating antigen processing and presentation machinery (20, 21); therefore, the role of IFN-γ in downregulating immune responses in the tumor microenvironment via induction of PD-L1 was not well accepted until more recently. This finding is vital to our current understanding of the unique immunology that takes place in the tumor microenvironment and provided an important clue that led to the “adaptive resistance” hypothesis (see below) that explains this pathway’s mechanism of action to evade tumor immunity.

Due to the lack of cell surface expression of PD-L1 on most cultured tumor lines, it is necessary to reexpress PD-L1 on the surface using transfection to recapitulate the effects of cell surface PD-L1 in human cancers and to create models to study how tumor-associated PD-L1 interacts with immune cells. We now know that cancer cells and other cells in the tumor microenvironment can upregulate the expression of PD-L1 after encountering T cells, mostly via IFN-γ, which may make the transfection-mediated expression of PD-L1 unnecessary in some tumor models. Nevertheless, our results demonstrated that PD-L1+ human tumor cells could eliminate activated effector T cells (Teffs) via apoptosis in coculture systems, and this effect could be blocked by inclusion of an anti-human PD-L1 mAb (clone 2H1). Next, we generated a hamster mAb (clone 10B5) against mouse PD-L1 to block its interaction with T cells and test its role in tumor immunity in vitro and in vivo. We demonstrated that progressive growth of PD-L1+ murine P815 tumors in syngeneic mice could be suppressed using anti–PD-L1 mAb (17). Altogether, these studies represented the initial attempt at using mAb to block the PD pathway as an approach for cancer therapy. These proof-of-concept studies (17) were confirmed by several subsequent studies. A study from Nagahiro Minato’s laboratory showed that the J558L mouse myeloma line constitutively expressed high levels of cell surface PD-L1 and the growth of these cells in syngeneic BALB/c mice could be partially suppressed by administering anti–PD-L1 mAb (22). Our laboratory showed that regression of progressively growing squamous cell carcinomas in syngeneic mice could also be suppressed using a combination of adoptively transferred tumor-draining lymphocytes and anti–PD-L1 mAb (23). Furthermore, the Zou laboratory demonstrated that ovarian cancer–infiltrating human T cells could be activated in vitro using DCs, which showed enhanced activity in the presence of anti–PD-L1 mAb; upon transfer, these cells could eliminate established human ovarian cancers in immune-deficient mice (24). These early studies established the concept that the PD pathway could be used by tumors to escape immune attack in the tumor microenvironment. More importantly, these studies built a solid foundation for the development of anti-PD therapy for the treatment of human cancers.  …..

Anti-PD therapy has taken center stage in immunotherapies for human cancer, especially for solid tumors. This therapy is distinct from the prior immune therapeutic agents, which primarily boost systemic immune responses or generate de novo immunity against cancer; instead, anti-PD therapy modulates immune responses at the tumor site, targets tumor-induced immune defects, and repairs ongoing immune responses. While the clinical success of anti-PD therapy for the treatment of a variety of human cancers has validated this approach, we are still learning from this pathway and the associated immune responses, which will aid in the discovery and design of new clinically applicable approaches in cancer immunotherapy.

 

PD-1 Pathway Inhibitors: Changing the Landscape of Cancer Immunotherapy

Dawn E. Dolan, PharmD, and Shilpa Gupta, MD

Background: Immunotherapeutic approaches to treating cancer have been evaluated during the last few decades with limited success. An understanding of the checkpoint signaling pathway involving the programmed death 1 (PD-1) receptor and its ligands (PD-L1/2) has clarified the role of these approaches in tumor-induced immune suppression and has been a critical advancement in immunotherapeutic drug development. Methods: A comprehensive literature review was performed to identify the available data on checkpoint inhibitors, with a focus on anti–PD-1 and anti–PD-L1 agents being tested in oncology. The search included Medline, PubMed, the ClinicalTrials.gov registry, and abstracts from the American Society of Clinical Oncology meetings through April 2014. The effectiveness and safety of the available anti–PD-1 and anti–PD-L1 drugs are reviewed. Results: Tumors that express PD-L1 can often be aggressive and carry a poor prognosis. The anti–PD-1 and anti–PD-L1 agents have a good safety profile and have resulted in durable responses in a variety of cancers, including melanoma, kidney cancer, and lung cancer, even after stopping treatment. The scope of these agents is being evaluated in various other solid tumors and hematological malignancies, alone or in combination with other therapies, including other checkpoint inhibitors and targeted therapies, as well as cytotoxic chemotherapy. Conclusions: The PD-1/PD-L1 pathway in cancer is implicated in tumors escaping immune destruction and is a promising therapeutic target. The development of anti–PD-1 and anti–PD-L1 agents marks a new era in the treatment of cancer with immunotherapies. Early clinical experience has shown encouraging activity of these agents in a variety of tumors, and further results are eagerly awaited from completed and ongoing studies.

……

Role of PD-1/PD-L1 Pathway PD-1 is an immunoinhibitory receptor that belongs to the CD28 family and is expressed on T cells, B cells, monocytes, natural killer cells, and many tumor-infiltrating lymphocytes (TILs)10; it has 2 ligands that have been described (PD-L1 [B7H1] and PD-L2 [B7-DC]).11 Although PD-L1 is expressed on resting T cells, B cells, dendritic cells, macrophages, vascular endothelial cells, and pancreatic islet cells, PD-L2 expression is seen on macrophages and dendritic cells alone.10 Certain tumors have a higher expression of PD-L1.12 PD-L1 and L2 inhibit T-cell proliferation, cytokine production, and cell adhesion.13 PD-L2 controls immune T-cell activation in lymphoid organs, whereas PD-L1 appears to dampen T-cell function in peripheral tissues.14 PD-1 induction on activated T cells occurs in response to PD-L1 or L2 engagement and limits effector T-cell activity in peripheral organs and tissues during inflammation, thus preventing autoimmunity. This is a crucial step to protect against tissue damage when the immune system is activated in response to infection.15-17 Blocking this pathway in cancer can augment the antitumor immune response.18 Like the CTLA-4, the PD-1 pathway down-modulates Tcell responses by regulating overlapping signaling proteins that are part of the immune checkpoint pathway; however, they function slightly differently.14,16 Although the CTLA-4 focuses on regulating the activation of T cells, PD-1 regulates effector T-cell activity in peripheral tissues in response to infection or tumor progression.16 High levels of CTLA-4 and PD-1 are expressed on regulatory T cells and these regulatory T cells and have been shown to have immune inhibitory activity; thus, they are important for maintaining self-tolerance.16 The role of the PD-1 pathway in the interaction of tumor cells with the host immune response and the PD-L1 tumor cell expression may provide the basis for enhancing immune response through a blockade of this pathway.16 Drugs targeting the PD-1 pathway may provide antitumor immunity, especially in PD-L1 positive tumors. Various cancers, such as melanoma, hepatocellular carcinoma, glioblastoma, lung, kidney, breast, ovarian, pancreatic, and esophageal cancers, as well as hematological malignancies, have positive PD-L1 expression, and this expression has been correlated with poor prognosis.8,19 Melanoma and kidney cancer are prototypes of immunogenic tumors that have historically been known to respond to immunotherapeutic approaches with interferon alfa and interleukin 2. The CTLA-4 antibody ipilimumab is approved by the US Food and Drug Administration for use in melanoma. Clinical activity of drugs blocking the PD-1/PD-L1 pathway has been demonstrated in melanoma and kidney cancer.20-24 In patients with kidney cancer, tumor, TIL-associated PD-L1 expression, or both were associated with a 4.5-fold increased risk of mortality and lower cancer-specific survival rate, even after adjusting for stage, grade, and performance status.18,19,25,26 A correlation between PD-L1 expression and tumor growth has been described in patients with melanoma, providing the rationale for using drugs that block the PD-1/PD-L1 pathway.19,27 Historically, immunotherapy has been ineffective in cases of non–small-cell lung cancer (NSCLC), which has been thought to be a type of nonimmunogenic cancer; nevertheless, lung cancer can evade the immune system through various complex mechanisms.28 In patients with advanced lung cancer, the peripheral and tumor lymphocyte counts are decreased, while levels of regulatory T cells (CD4+), which help suppress tumor immune surveillance, have been found at higher levels.29-32 Immune checkpoint pathways involving the CTLA-4 or the PD-1/PD-L1 are involved in regulating T-cell responses, providing the rationale for blocking this pathway in NSCLC with antibodies against CTLA-4 and the PD-1/PD-L1 pathway.32 Triple negative breast cancer (TNBC) is an aggressive subset of breast cancer with limited treatment options. PD-L1 expression has been reported in patients with TNBC. When PD-L1 expression was evaluated in TILs, it correlated with higher grade and larger-sized tumors.33 Tumor PD-L1 expression also correlates with the infiltration of T-regulatory cells in TNBC, findings that suggest the role of PD-L1–expressing tumors and the PD-1/PD-L1–expressing TILs in regulating immune response in TNBC.34

…….

Preclinical evidence exists for the complementary roles of CTLA-4 and PD-1 in regulating adaptive immunity, and this provides rationale for combining drugs targeting these pathways.44-46 Paradoxically and originally believed to be immunosuppressive, new data allow us to recognize that cytotoxic agents can antagonize immunosuppression in the tumor microenvironment, thus promoting immunity based on the concept that tumor cells die in multiple ways and that some forms of apoptosis may lead to an enhanced immune response.8,15 For example, nivolumab was combined with ipilimumab in a phase 1 trial of patients with advanced melanoma.46 The combination had a manageable safety profile and produced clinical activity in the majority of patients, with rapid and deep tumor regression seen in a large proportion of patients. Based on the results of this study, a phase 3 study is being undertaken to evaluate whether this combination is better than nivolumab alone in melanoma (NCT01844505). Several other early-phase studies are underway to explore combinations of various anti–PD-1/PD-L1 drugs with other therapies across a variety of tumor types (see Tables 1 and 2), possibly paving the way for future combination studies.

 

Development of PD-1/PD-L1 Pathway in Tumor Immune Microenvironment and Treatment for Non-Small Cell Lung Cancer

Jiabei He, Ying Hu, Mingming Hu & Baolan Li

Lung cancer is currently the leading cause of cancer-related death in worldwide, non-small cell lung cancer (NSCLC) accounts for about 85% of all lung cancers. Surgery, platinum-based chemotherapy, molecular targeted agents and radiotherapy are the main treatment of NSCLC. With the strategies of treatment constantly improving, the prognosis of NSCLC patients is not as good as before, new sort of treatments are needed to be exploited. Programmed death 1 (PD-1) and its ligand PD-L1 play a key role in tumor immune escape and the formation of tumor microenvironment, closely related with tumor generation and development. Blockading the PD-1/PD-L1 pathway could reverse the tumor microenvironment and enhance the endogenous antitumor immune responses. Utilizing the PD-1 and/or PD-L1 inhibitors has shown benefits in clinical trials of NSCLC. In this review, we discuss the basic principle of PD-1/PD-L1 pathway and its role in the tumorigenesis and development of NSCLC. The clinical development of PD-1/PD-L1 pathway inhibitors and the main problems in the present studies and the research direction in the future will also be discussed.

Lung cancer is currently the leading cause of cancer-related death in the worldwide. In China, the incidence and mortality of lung cancer is 5.357/10000, 4.557/10000 respectively, with nearly 600,000 new cases every year1. Non-small cell lung cancer (NSCLC) accounts for about 85% of all lung cancers, the early symptoms of patients with NSCLC are not very obvious, especially the peripheral lung cancer. Though the development of clinic diagnostic techniques, the majority of patients with NSCLC have been at advanced stage already as they are diagnosed. Surgery is the standard treatment in the early stages of NSCLC, for the advanced NSCLC, the first-line therapy is platinum-based chemotherapy. In recent years, patients with specific mutations may effectively be treated with molecular targeted agents initially. The prognosis of NSCLC patients is still not optimistic even though the projects of chemotherapy as well as radiotherapy are continuously ameliorating and the launch of new molecular targeted agents is never suspended, the five-year survival rate of NSCLC patients is barely more than 15%2, the new treatment is needed to be opened up.

During the last few decades, significant efforts of the interaction between immune system and immunotherapy to NSCLC have been acquired. Recent data have indicated that the lack of immunologic control is recognized as a hallmark of cancer currently. Programmed death-1 (PD-1) and its ligand PD-L1 play a key role in tumor immune escape and the formation of tumor microenvironment, closely related with tumor generation and development. Blockading the PD-1/PD-L1 pathway could reverse the tumor microenvironment and enhance the endogenous antitumor immune responses.

In this review, we will discuss the PD-1/PD-L1 pathway from the following aspects: the basic principle of PD-1/PD-L1 pathway and its role in the tumorigenesis and development of NSCLC, the clinical development of several anti-PD-1 and anti-PD-L1 drugs, including efficacy, toxicity, and application as single agent, or in combination with other therapies, the main problems in the present studies and the research direction in the future.

 

Cancer as a chronic, polygene and often inflammation-provoking disease, the mechanism of its emergence and progression is very complicated. There are many factors which impacted the development of the disease, such as: environmental factors, living habits, genetic mutations, dysfunction of the immune system and so on. At present, increasing evidence has revealed that the development and progression of tumor are accompanied by the formation of special tumor immune microenvironment. Tumor cells can escape the immune surveillance and disrupt immune checkpoint of host in several methods, therefore, to avoid the elimination from the host immune system. Human cancers contain a number of genetic and epigenetic changes, which can produce neoantigens that are potentially recognizable by the immune system3, thus trigger the body’s T cells immune response. The T cells of immune system recognize cancer cells as abnormal primarily, generate a population of cytotoxic T lymphocytes (CTLs) that can traffic to and infiltrate cancers wherever they reside, and specifically bind to and then kill cancer cells. Effective protective immunity against cancer depends on the coordination of CTLs4. Under normal physiological conditions, there is a balance status in the immune checkpoint molecule which makes the immune response of T cells keep a proper intensity and scope in order to minimize the damage to the surrounding normal tissue and avoid autoimmune reaction. However, numerous pathways are utilized by cancers to up-regulate the negative signals through cell surface molecules, thus inhibit T-cell activation or induce apoptosis and promote the progression and metastasis of cancers5. Increasing experiments and clinical trails show that immunotherapeutic approaches utilizing antagonistic antibodies to block checkpoint pathways, can release cancer inhibition and facilitate antitumor activity, so as to achieve the purpose of treating cancer.

The present research of immune checkpoint molecules are mainly focus on cytotoxic T lymphocyte-associated antigen 4 (CLTA-4), Programmed death-1 (PD-1) and its ligands PD-L1 (B7H1) and PD-L2 (B7-DC). CTLA-4 regulates T cell activity in the early stage predominantly, and PD-1 mainly limits the activity of T-cell in the tumor microenvironment at later stage of tumor growth6. Utilizing the immune checkpoint blockers to block the interactions between PD-1 and its ligands has shown benefits in clinical trials, including the NSCLC patients. PD-1 and its ligands have been rapidly established as the currently most important breakthrough targets in the development of effective immunotherapy.

PD-1/PD-L1 pathway and its expression, regulation

PD-1 is a type 1 trans-membrane protein that encoded by the PDCD1 gene7. It is a member of the extended CD28/CTLA-4 immunoglobulin family and one of the most important inhibitory co-receptors expressed by T cells. The structure of the PD-1 includes an extracellular IgV domain, a hydrophobic trans-membrane region and an intracellular domain. The intracellular tail includes separate potential phosphorylation sites that are located in the immune receptor tyrosine-based inhibitory motif (ITIM) and in the immunoreceptor tyrosine-based switch motif (ITSM). Mutagenetic researches indicated that the activated ITSM is essential for the PD-1 inhibitory effect on T cells8. PD-1 is expressed on T cells, B cells, monocytes, natural killer cells, dendritic cells and many tumor-infiltrating lymphocytes (TILs)9. In addition, the research of Francisoet et al. showed that PD-1 was also expressed on regulatory T cells (Treg) and able to facilitate the proliferation of Treg and restrain immune response10.

PD-1 has two ligands: PD-L1 (also named B7-H1; CD274) and PD-L2 (B7-DC; CD273), that are both coinhibitory. PD-L1 is expressed on resting T cells, B cells, dendritic cells, macrophage, vascular endothelial cells and pancreatic islet cells. PD-L2 expression is seen on macrophages and dendritic cells alone and is far less prevalent than PD-L1 across tumor types. It shows much more restricted expression because of its more restricted tissue distribution. Differences in expression patterns suggest distinct functions in immune regulation across distinct cell types. The restricted expression of PD-L2, largely to antigen-presenting cells, is consistent with a role in regulating T-cell priming or polarization, whereas broad distribution of PD-L1 suggests a more general role in protecting peripheral tissues from excessive inflammation.

PD-L1 is expressed in various types of cancers, especially in NSCLC11,12, melanoma, renal cell carcinoma, gastric cancer, hepatocellular as well as cutaneous and various leukemias, multiple myeloma and so on13,14,15. It is present in the cytoplasm and plasma membrane of cancer cells, but not all cancers or all cells within a cancer express PD-L116,17. The expression of PD-L1 is induced by multiple proinflammatory molecules, including types I and II IFN-γ, TNF-α, LPS, GM-CSF and VEGF, as well as the cytokines IL-10 and IL-4, with IFN-γ being the most potent inducer18,19. IFN-γ and TNF-α are produced by activated type 1 T cells, and GM-CSF and VEGF are produced by a variety of cancer stromal cells, the tumor microenvironment upregulates PD-L1 expression, thereby, promotes immune suppression. This latter effect is called “adaptive immune resistance”, because the tumor protects itself by inducing PD-L1 in response to IFN-γ produced by activated T cells17. PD-L1 is regulated by oncogenes, also known as the inherent immune resistance. PD-L1 expression is suppressed by the tumor suppressor gene: PTEN (phosphatase and tension homolog deleted on chromosome ten) gene. Cancer cells frequently contain mutated PTEN, which can activate the S6K1 gene, thus results in PD-L1 mRNA to polysomes increase greatly20, hence increases the translation of PD-L1 mRNA and plasma membrane expression of PD-L1. Parsa et al.’s research also demonstrated that neuroglioma with PTEN gene deletion regulate PD-L1 expression at the translational level by activating the PI3K/AKT downstream mTOR-S6K1signal pathway and, hence increase the PD-L1 expression21. Micro-RNAs also translationally regulate PD-L1 expression. MiRNA-513 is complementary to the 3′ untranslated region of PD-L1 and prevents PD-L1 mRNA translation22. In addition, a later literature reported that in the model of melanoma, the up-regulation of PD-L1 is closely related to the CD8 T cell, independent of regulation by oncogenes13. Noteworthily, the PD-L1 can bind to T cell expressed CD80, and at this point CD80 is a receptor instead of ligand to transmit negative regulated signals23.

 

PD-1/PD-L1 mediate immune suppression by multiple mechanisms

Like the CTLA-4, the PD-1/PD-L1 pathway down-modulates T-cell response by regulating overlapping signal proteins in the immune checkpoint pathway. However, their functions are slightly different24. The CTLA-4 focuses on regulating the activation of T cells, while PD-1 regulates effector T-cell activity in peripheral tissues in response to infection or tumor progression25. Tregs that high-level expression of PD-1 have been shown to have immune inhibitory activity, thus, they are important for maintaining self-tolerance. In normal human bodies, this is a crucial step to protect against tissue damage when the immune system is activated in response to infection26. However, in response to immune attack, cancer cells overexpress PD-L1 and PD-L2. They bind to PD-1 receptor on T cells, inhibiting the activation of T-cells, thus suppressing T-cell attack and inducing tumor immune escape. Thus tumor cells effectively form a suitable tumor microenvironment and continue to proliferate27. PD-1/PD-L1 pathway regulates immune suppression by multiple mechanisms, specific performance of the following: Induce apoptosis of activated T cells: PD-1 reduces T cell survival by impacting apoptotic genes. During T cell activation, CD28 ligation sustains T cell survival by driving expression of the antiapoptotic gene Bcl-xL. PD-1 prevents Bcl-xL expression by inhibiting PI3K activation, which is essential for upregulation of Bcl-xL. Early studies demonstrated that PD-L1+ murine and human tumor cells induce apoptosis of activated T cells and that antibody blocking of PD-L1 can decrease the apoptosis of T cells and facilitate antitumor immunity28,16. Facilitate T cell anergy and exhaustion: A research shown that the occurrence of tumor is associated with chronic infection29. According to the study of chronic infection, PD-1 overexpressed on the function exhausted T cells, blocking the PD-1/PD-L1 pathway can restore the proliferation, secretion and cytotoxicity30. In addition, later research demonstrated that the exhaustion of TILs in the tumor microenvironment is closely related to the PD-L1 expression of tumor cells, myeloid cells derived from tumor31. Enhance the function of regulatory T cells: PD-L1 can promote the generation of induced Tregs by down-regulating the mTOR, AKT, S6 and the phosphorylation of ERK2 and increasing PTEN, thus restrain the activity of effector T-cell32. Blocking the PD-1/PD-L1 pathway can increase the function of effector CD8 T-cell and inhibt the function of Tregs, bone marrow derived inhibition cells, thus enhance the anti-tumor response. Inhibit the proliferation of T cells: PD-1 ligation also prevents phosphorylation of PKC-theta, which is essential for IL-2 production33, and arrests T cells in the G1 phase, blocking proliferation. PD-1 mediates this effect by activating Smad3, a factor that arrests cycling34. Restrain impaired T cell activation and IL-2 production: PD-1/PD-L1 blocks the downstream signaling events triggered by Ag/MHC engagement of the TCR and co-stimulation through CD28, resulting in impaired T cell activation and IL-2 production. Signaling through the TCR requires phosphorylation of the tyrosine kinase ZAP70. PD-1 engagement reduces the phosphorylation of ZAP70 and, hence, inhibits downstream signaling events. In addition, signaling through PD-1 also prevents the conversion of functional CD8+ T effector memory cells into CD8+ central memory cells35 and, thus, reduces long-term immune memory that might protect against future metastatic disease. PD-L1 also promotes tumor progression by reversing signaling through CD80 into T cells. CD80-PD-L1 interactions restrain self-reactive T cells in an autoimmune setting36, therefore, their inhibition may facilitate antitumor immunity.

Researches on the mechanism of PD-1/PD-L1 pathway mediating immune escape are still ongoing, especially the mechanism of PD-L2 is still unclear. These researches provide the theoretical basis and research direction for the further immunotherapy targets research.

 

Anti-PD-1 antibodies

Nivolumab

Nivolumab (BMS-936558, Brand name: Opdivo) is a human monoclonal IgG4 antibody that essentially lacks detectable antibody-dependent cellular cytotoxicity (ADCC). Inhibition by monoclonal antibody of PD-1 on CD8+ TILs within lung cancers can restore cytokine secretion and T-cell proliferation48. Results of a larger phase I study in 296 patients (236 patients evaluated) reported that the objective response (complete or partial responses) of patients with NSCLC was 18%. A total of 65% of responders had durable responses lasting for more than 1 year. Stable disease lasting 24 weeks was seen in patients with NSCLC. PD-L1expression was tested in 42 patients: 9 of 25(36%) patients whose PD-L1 expression positive were objectively response to PD-1 blockade treatment, while the remaining 17 nonresponsive patients were negative45.

In another early phase I trial of nivolumab49, an objective response was observed in 22 patients (17%; 95% CI, 11%–25%) in a dose-expansion cohort of 129 previously treated patients with advanced NSCLC. Six additional patients who had an unconventional immune-related response were not included. Moreover, the median duration of response was exceptional for 17 months. Although the median PFS in the cohort was 2.3 months and the median overall survival was 9.9 months, it seemed clear that those who responded had sustained benefit. Specifically, the 2-year overall survival rate was 24%, and many remained in remission after completing 96 weeks of continuous therapy.

Single-agent trials of nivolumab are planning or ongoing on NSCLC (NCT01721759, NCT02066636). In addition, there are clinical randomized trials which focus on the comparison of nivolumab and plain-based combination chemotherapy (NCT02041533, NCT01673867). In March 4, 2015, nivolumab was approved by the US Food and Drug Administration for treatment of patients with metastatic NSCLC (squamous cell carcinoma), when progression of their diseases during or after chemotherapy with platinum-based drugs.

Pembrolizumab

Pembrolizumab (MK-3475) is a highly selective, humanized monoclonal antibody with activity against PD-1 that contains a mutation at C228P designed to prevent Fc-mediated ADCC. It is now in the clinical research phases for patients with advanced solid tumors. Its safety and efficacy were evaluated in a phase I clinical trial of KEYNOTE-001. The best response according of 38 cases of patients which initially accepted pembrolizumab 10 mg/kg q3wwas 21% (based on RECIST1.1 evaluation) and the median PFS of responder still has not reached until 62 weeks. The researchers also found that the antitumor activity of pembrolizumab was associated with the PD-L1expression44,50. The critical values of the expression of PD-L1 will be validated in 300 cases of patients which will soon been rolled into the study.

Clinical trial of pembrolizumab monotherapy is ongoing for patients with NSCLC (NCT01840579). Randomized trials comparing pembrolizumab to combination chemotherapy (NCT02142738) or single-agent docetaxel (NCT01905657) are ongoing in PD-L1 positive patients with NSCLC.

Pidilizumab (CT-011)

Pidilizumab is a humanized IgG-1K recombinant anti-PD-1 monoclonal antibody that has demonstrated antitumor activity in mouse cancer models. In a first-in-human phase I dose-escalation study in patients with only advanced hematologic cancers, there is no clinical trials of NSCLC presently51.

 

Anti-PD-L1 antibodies

Another therapeutic method based on the PD-1/PD-L1 pathway is by specific binding between antibody and PD-L1, thus preventing its activity. It was speculated that utilizing PD-L1 as therapeutic target maybe accompanied by less toxicity in part by modulating the immune response selectively in the tumor microenvironment. However, since PD-L2 expressed by tumor cells or some other tumor-associated molecules may play a role in mediating PD-1-expressing lymphocytes, it is conceivable that the magnitude of the anti-tumor immune response could also be blunted.

BMS-936559

BMS-936559/MDX1105 is a fully humanized, high affinity, IgG4 monoclonal antibody that react specifically with PD-L1, thus inhibiting the binding of PD-L1 and PD-1, CD80 (which binds not only PD-L1 but also CTLA-4 and CD28). Initial results from a multicenter and dose-escalation phase I trial of 207 patients(including 75 cases of patients with NSCLC) showed durable tumor regression (objective response rate of 6%–17%) and prolonged stabilization of disease (12%–41% at 24weeks) in patients with advanced cancers, including NSCLC, melanoma and kidney cancer. In patients with NSCLC, there were five objective responses (in 4 patients with the nonsquamous subtype and 1 with the squamous subtype) at doses of 3 mg/kg and 10 mg/kg, with response rates of 8% and 16%, respectively. Six additional patients with NSCLC had stable disease lasting at least 24 weeks52.

MPDL3280A

MPDL3280A is a human IgG1 antibody that targets PD-L1. Its Fc component has been engineered to not activate antibody-dependent cell cytotoxicity. In a recently reported phase I study, a 21% response rate was noted in patients with metastatic melanoma, RCC or NSCLC53, including several patients who demonstrated shrinkage of tumor within a few days of initiating treatment.

Fifty-two patients were enrolled in an expansion cohort of the phase I trial of MPDL3280A, 62% of them were heavily pretreated NSCLC (≥3 lines of systemic therapy) and the ORR was 22%54. Analysis of biomarker data from archival tumor samples demonstrated a correlation between PD-L1 status and response and lack of progressive disease55.

MEDI4736

MEDI4736 is a human IgG1 antibody that binds specifically to PD-L1, thus preventing PD-L1 binding to PD-1 and CD80. Interim results from a phase I trial reported no colitis or pneumonitis of any grade, with several durable remissions, including NSCLC patients56. An ongoing phase I dose-escalation study (NCT01693562) of MEDI-4736 in 26 patients, 4 partial responses (3 in patients with NSCLC and 1 with melanoma) were observed and 5 additional patients exhibited lesser degrees of tumor shrinkage. The disease control rate at 12 weeks was 46%57. Expansion cohorts was opened in Sep 2013, 10 mg/kg q2w dose. 151 patients was enrolled so far in the expansion cohorts, tumor shrinkage was reported as early as the first assessment at 6 weeks and among the 13 patients with NSCLC, responses were sustained at 10 or more to 14.9 or more months58. In the NSCLC expansion cohort, the response rate was 16% in 58 evaluable patients and the disease control rate at 12 weeks was 35% with responses seen in all histologic subtypes as well as in a smaller proportion of PD-L1- tumors.

On the basis of the favorable toxicity profile and promising activity in a heavily pretreated NSCLC population, a global Phase III placebo controlled trial using the 10 mg/kg biweekly dose has been launched in Stage III patients who have not progressed following chemo-radiation (NCT02125461). The primary outcome measures are overall survival and progression-free survival.

AMP-224

AMP-224 was a B7-DC-Fc fusion protein which can block the PD-1 receptor competitively59. Some NSCLC patients were included in a first-in-man phase I trial of this fusion protein drug. A dose-dependent reduction in PD-1-high TILs was observed at 4 hours and 2 weeks after drug administration60.

 

A variety of approaches for combining PD-1/PD-L1 pathway inhibitors with other therapeutic methods have been explored over the past few years in an effort to offer more feasible therapeutic options for clinic to improve treatment outcomes. Approaches have included combinations with other immune checkpoint inhibitors, immunostimulatory cytokines (e.g. IFN-y) cytotoxic chemotherapy, platinum-based chemotherapy, radiotherapy, anti-angiogenic inhibitors, tumor vaccine and small-molecule molecularly targeted therapies many with promising results61,62. Studies indicated that PD-1/PD-L1 pathway inhibitors were most effective when combined with treatments that activating the immune system63.

Preclinical evidence exists for the complementary roles of CTLA-4 and PD-1 in regulating adaptive immunity, and this provides rationale for combining drugs targeting these pathways. In a Phase I study in 46 chemotherapy-naive patients with NSCLC, four cohorts of patients received ipilimumab (3 mg/kg) plus nivolumab for four cycles followed by nivolumab 3 mg/kg intravenously every 2 weeks. The ORR was 22% and did not correlate with PD-L1 status64.

In another Phase I study, 56 patients with advanced NSCLC were assigned based on histology to four cohorts to receive nivolumab (5–10 mg/kg) intravenously every 3 weeks plus one of four concurrent standard “platinum doublet” chemotherapy regimens. No dose de-escalation was required for dose-limiting toxicity. The ORR was 33–50% across arms and the 1-year OS rates were promising at 59–87%65.

…..

The research of cancer immunotherapy provides a new wide space for cancer treatment (including NSCLC), and compared with other therapeutic method, immunotherapy has its unique advantages, such as: relative safety, effectivity, less and low grade side effect and so on. Especially with the discovery and continued in-depth study of PD-1/PD-L1 pathway in the immune regulation mechanism, many significative conclusions were reported. Data from many clinical trails suggest that some patients with NSCLC have been benefited from the drugs of anti-PD-1 and anti-PD-L1 already. However, summarized what have been discussed above, only a small fraction of patients benefit from PD-1 or PD-L1 inhibitors treatment. But with the continuous studies on biomarker and combined treatment in PD-1/PD-L1 pathway, new research progress will be acquired as well. We will make significant progress on treatment and in control of NSCLC.

 

Prospects for Targeting PD-1 and PD-L1 in Various Tumor Types     

Table 1: Selected Anti–PD-1 and Anti–PD-L1 Antibodies
Table 2: Selected Adverse Events
Table 3: Selected Clinical Trials for Metastatic Melanoma
Table: 4 Selected Trials for Metastatic Renal Cell Carcinoma
Table 5: Selected Trials for Non–Small-Cell Lung Cancer (NSCLC )
Table 6: Selected Trials for Other Tumor Types

Immune checkpoints, such as programmed death ligand 1 (PD-L1) or its receptor, programmed death 1 (PD-1), appear to be Achilles’ heels for multiple tumor types. PD-L1 not only provides immune escape for tumor cells but also turns on the apoptosis switch on activated T cells. Therapies that block this interaction have demonstrated promising clinical activity in several tumor types. In this review, we will discuss the current status of several anti–PD-1 and anti–PD-L1 antibodies in clinical development and their direction for the future.

Several PD-1 and PD-L1 antibodies are in clinical development (Table 1). Overall, they are very well tolerated; most did not reach dose-limiting toxicity in their phase I studies. As listed in Table 2, no clinically significant difference in adverse event profiles has been seen between anti–PD-1 and anti–PD-L1 antibodies. Slightly higher rates of infusion reactions (11%) were observed with BMS-936559 (anti–PD-L1) than with BMS-96558 (nivolumab). In an early stage of a nivolumab phase I study, there was concern about fatal pneumonitis.[7] It has been hypothesized that PD-1 interaction with PD-L2 expressed on the normal parenchymal cells of lung and kidney provides unique negative signaling that prevents autoimmunity.[8] Thus, anti–PD-1 antibody blockage of such an interaction may remove this inhibition, allowing autoimmune pneumonitis or nephritis. Anti–PD-L1 antibody, however, would theoretically leave PD-1–PD-L2 interaction intact, preventing the autoimmunity caused by PD-L2 blockade. With implementation of an algorithm to detect early signs of pneumonitis and other immune-related adverse events, many of these side effects have become manageable. However, it does require discerning clinical attention to detect potentially fatal side effects. In terms of antitumor activity, both anti–PD-1 and anti–PD-L1 antibodies have shown responses in overlapping multiple tumor types. Although limited to a fraction of patients, most responses, when observed, were rapid and durable.

– See more at: http://www.cancernetwork.com/oncology-journal/prospects-targeting-pd-1-and-pd-l1-various-tumor-types#sthash.an8uOYLi.dpuf

 

Immune Checkpoint Blockade in Cancer Therapy

Michael A. PostowMargaret K. Callahan and Jedd D. Wolchok
http://jco.ascopubs.org/content/early/2015/01/20/JCO.2014.59.4358.full
 http://dx.doi.org:/10.1200/JCO.2014.59.4358

Immunologic checkpoint blockade with antibodies that target cytotoxic T lymphocyte–associated antigen 4 (CTLA-4) and the programmed cell death protein 1 pathway (PD-1/PD-L1) have demonstrated promise in a variety of malignancies. Ipilimumab (CTLA-4) and pembrolizumab (PD-1) are approved by the US Food and Drug Administration for the treatment of advanced melanoma, and additional regulatory approvals are expected across the oncologic spectrum for a variety of other agents that target these pathways. Treatment with both CTLA-4 and PD-1/PD-L1 blockade is associated with a unique pattern of adverse events called immune-related adverse events, and occasionally, unusual kinetics of tumor response are seen. Combination approaches involving CTLA-4 and PD-1/PD-L1 blockade are being investigated to determine whether they enhance the efficacy of either approach alone. Principles learned during the development of CTLA-4 and PD-1/PD-L1 approaches will likely be used as new immunologic checkpoint blocking antibodies begin clinical investigation.

CTLA-4 was the first immune checkpoint receptor to be clinically targeted (Fig 1) Normally, after T-cell activation, CTLA-4 is upregulated on the plasma membrane where it functions to downregulate T-cell function through a variety of mechanisms, including preventing costimulation by outcompeting CD28 for its ligand, B7, and also by inducing T-cell cycle arrest.15 Through these mechanisms and others, CTLA-4 has an essential role in maintaining normal immunologic homeostasis, as evidenced by the fact that mice deficient in CTLA-4 die from fatal lymphoproliferation.6,7 Recognizing the role of CTLA-4 as a negative regulator of immunity, investigators led studies demonstrating that antibody blockade of CTLA-4 could result in antitumor immunity in preclinical models.8,9

Fig 1.

IMAGE SOURCE:

http://ascopubs.org/doi/figure/10.1200/JCO.2014.59.4358

Article SOURCE:

http://jco.ascopubs.org/content/early/2015/01/20/JCO.2014.59.4358/F1.medium.gif

Fig 1.

The cytotoxic T lymphocyte–associated antigen 4 (CTLA-4) immunologic checkpoint. T-cell activation requires antigen presentation in the context of a major histocompatibility complex (MHC) molecule in addition to the costimulatory signal achieved when B7 on an antigen-presenting cell (dendritic cell shown) interacts with CD28 on a T cell. Early after activation, to maintain immunologic homeostasis, CTLA-4 is translocated to the plasma membrane where it downregulates the function of T cells.

On the basis of this preclinical rationale, two antibodies targeting CTLA-4, ipilimumab (Bristol-Myers Squibb, Princeton, NJ) and tremelimumab (formerly Pfizer, currently MedImmune/AstraZeneca, Wilmington, DE), entered clinical development. Early reports of both agents showed durable clinical responses in some patients.1012Unfortunately, despite a proportion of patients experiencing a durable response, tremelimumab did not statistically significantly improve overall survival, which led to a negative phase III study comparing tremelimumab to dacarbazine/temozolomide in patients with advanced melanoma.13 It is possible that the lack of an overall survival benefit was a result of the crossover of patients treated with chemotherapy to an expanded access ipilimumab program or a result of the dosing or scheduling considerations of tremelimumab.

Ipilimumab, however, was successful in improving overall survival in two phase III studies involving patients with advanced melanoma.14,15 Although the median overall survival was only improved by several months in each of these studies, landmark survival after treatment initiation favored ipilimumab; in the first phase III study, 18% of patients were alive after 2 years compared with 5% of patients who received the control treatment of gp100 vaccination.14 More recently reported pooled data from clinical trials of ipilimumab confirm that approximately 20% of patients will have long-term survival of at least 3 years after ipilimumab therapy, with the longest reported survival reaching 10 years.1618

For patients with other malignancies, CTLA-4 antibody therapy has also shown some benefits. Ipilimumab, in combination with carboplatin and paclitaxel in a phased treatment schedule, showed improved progression-free survival compared with carboplatin and paclitaxel alone for patients with non–small-cell lung cancer.19Several patients with pancreatic cancer had declines in CA 19-9 when ipilimumab was given with GVAX (Aduro, Berkeley, CA),20and ipilimumab has also resulted in responses in patients with prostate cancer.21 Unfortunately, a phase III study in patients with castrate-resistant prostate cancer who experienced progression on docetaxel chemotherapy demonstrated that after radiotherapy, ipilimumab did not improve overall survival compared with placebo.22 Although this study is felt to have been a negative study, ipilimumab may have conferred a benefit to patients with favorable prognostic features, such as the absence of visceral metastases, but this requires further study. Another CTLA-4–blocking antibody, tremelimumab, has shown responses in patients with mesothelioma, and ongoing trials are under way.23

CTLA-4 blockade has also been administered together with other immunologic agents, such as the indoleamine 2,3-dioxygenase inhibitor INCB024360,106 the oncolytic virus talimogene laherparepvec,107 and granulocyte-macrophage colony-stimulating factor,108 with encouraging early results. We expect subsequent studies involving engineered T-cell–based therapies and checkpoint blockade.

Other promising data involve CTLA-4 combinations with PD-1 blockade. A phase I study of ipilimumab and nivolumab in patients with melanoma resulted in a high durable response rate and impressive overall survival compared with historical data.109,110Although the most recently reported grade 3 or 4 toxicity rate in patients with melanoma was 64%, which is higher than either ipilimumab or nivolumab individually,111 the vast majority of these irAEs were asymptomatic laboratory abnormalities of unclear clinical consequence. For example, elevations in amylase or lipase were reported in 21% of patients, none of whom met clinical criteria for a diagnosis of pancreatitis. The rate of grade 3 or 4 diarrhea was 7%, which is approximately similar to the rate of grade 3 or 4 diarrhea with ipilimumab monotherapy at 3 mg/kg. Whether ipilimumab and nivolumab improve overall survival compared with either nivolumab or ipilimumab alone remains the subject of an ongoing phase III randomized trial, and investigations of the combination of ipilimumab and nivolumab (and tremelimumab and MEDI4736) are ongoing in many other cancers.

Immunotherapy with checkpoint-blocking antibodies targeting CTLA-4 and PD-1/PD-L1 has improved the outlook for patients with a variety of malignancies. Despite the promise of this approach, many questions remain, such as the optimal management of irAEs and how best to evaluate combination approaches to determine whether they will increase the efficacy of CTLA-4 or PD-1/PD-L1 blockade alone. Themes from the experience with CTLA-4 and PD-1/PD-L1 will likely be relevant for investigations of novel immunologic checkpoints in the future.

This is a very important article, Dr. Larry.

It fits so beautiful with our work on Molecules in Development Table.

Thank you

 

This image depicts the process of metastasis in a mouse tumor, where tumor cells (green) have helped to reorganize the collagen into aligned fibers (blue) that provide the structural support for motility. This helps the tumor cells to enter blood vessels (red), ultimately leading to the formation of metastases in other organs.

http://news.mit.edu/sites/mit.edu.newsoffice/files/styles/news_article_image_top_slideshow/public/images/2016/MIT-Cancer-Migration-1_0.jpg?itok=aEOCRQpn

This image depicts the process of metastasis in a mouse tumor, where tumor cells (green) have helped to reorganize the collagen into aligned fibers (blue) that provide the structural support for motility. This helps the tumor cells to enter blood vessels (red), ultimately leading to the formation of metastases in other organs.  Image: Madeleine Oudin and Jeff Wyckoff

Paving the way for metastasis

Cancer cells remodel their environment to make it easier to reach nearby blood vessels.

Anne Trafton | MIT News Office     March 15, 2016

 

A new study from MIT reveals how cancer cells take some of their first steps away from their original tumor sites. This spread, known as metastasis, is responsible for 90 percent of cancer deaths.

Studying mice, the researchers found that cancer cells with a particular version of the Mena protein, called MenaINV (invasive), are able to remodel their environment to make it easier for them to migrate into blood vessels and spread through the body. They also showed that high levels of this protein are correlated with metastasis and earlier deaths among breast cancer patients.

Finding a way to block this protein could help to prevent metastasis, says Frank Gertler, an MIT professor of biology and a member of the Koch Institute for Integrative Cancer Research.

“That’s something that I think would be very promising, because we know that when we genetically remove MenaINV, the tumors become nonmetastatic,” says Gertler, who is the senior author of a paper describing the findings in the journal Cancer Discovery.

Madeleine Oudin, a postdoc at the Koch Institute, is the paper’s lead author.

On the move

For cancer cells to metastasize, they must first become mobile and then crawl through the surrounding tissue to reach a blood vessel. In the new study, the MIT team found that cancer cells follow the trail of fibronectin, a protein that is part of the “extracellular matrix” that provides support for surrounding cells. Fibronectin is found in particularly high concentrations around the edges of tumors and near blood vessels.

“Cancer cells within a tumor environment are constantly faced with differences in fibronectin concentrations, and they need to be able to move from low to high concentrations to reach the blood vessels,” Oudin says.

MenaINV, an alternative form of the normal Mena protein, is key to this process. MenaINV includes a segment not found in the normal version, and this makes it bind more strongly to a receptor known as alpha-5 integrin, which is found on the surfaces of tumor cells and nearby supporting cells, and recognizes fibronectin.

When MenaINV attaches to this receptor, it promotes the binding of fibronectin to the same receptors. Fibronectin is normally a tangled protein, but when it binds to cell surfaces, it gets stretched out into long bundles. This stimulates the organization of collagen, another extracellular matrix protein, into stiff fibrils that radiate from the edges of the tumor.

This pattern, which is typically seen in tumors that are more aggressive, essentially paves the way for tumor cells to move toward blood vessels.

“If you have curly, coiled collagen, that’s associated with a good outcome, but if it gets realigned into these really straight long fibers, that provides highways for these cells to migrate on,” Oudin says.

In studies of mice, cells with the invasive form of Mena were better able to recognize and crawl toward higher concentrations of fibronectin, moving along the collagen pathways, while cells without MenaINV did not move toward the higher concentrations.

Predicting metastasis

The researchers also looked at data from breast cancer patients and found that high levels of MenaINV and fibronectin are associated with metastasis and earlier death. However, there was no link between the normal version of Mena and earlier death.

Gertler’s lab had previously developed antibodies that can detect the normal and invasive forms of Mena, which are now being developed for testing patient biopsy samples. Such tests could help doctors to determine whether a patient’s tumor is likely to spread or not, and possibly to guide the patient’s treatment. In addition, scientists may be able to develop drugs that inhibit MenaINV, which could be useful for treating cancer or preventing it from metastasizing.

The researchers now hope to study how MenaINV may contribute to other types of cancers. Preliminary studies suggest that it plays a similar role in lung and colon cancers as that seen in breast cancer. They are also investigating how the choice between the two forms of the Mena protein is regulated, and how other proteins found in the extracellular matrix might contribute to cancer cell migration.

Facilitating Tumor Cell Migration

Researchers identify a modified form of a migration-regulating protein in cancer cells that remodels the tumor microenvironment to promote metastasis.
By Catherine Offord | March 16, 2016

Emerging evidence suggests that metastasis—the spread of cancer from one organ or tissue to another—is aided by a significant remodeling of the cancer cells’ surroundings. Now, researchers at MIT have made progress toward understanding the mechanisms involved in this process by highlighting the role of a protein that reorganizes the tumor’s extracellular matrix to facilitate cellular migration into blood vessels. The findings were published yesterday (March 15) in Cancer Discovery.

Using a mouse model, the team showed that a cancer-cell-expressed protein called MenaINV—a mutated, “invasive” form of the cell-migration-modulator Mena—binds more strongly than its normal equivalent to a receptor on tumor and nearby support cells. The binding rearranges fibronectin in the tumor microenvironment, which in turn triggers the reorganization of collagen in the extracellular matrix into linear fibers radiating from the tumor.

This collagen restructuring is key in facilitating the migration of tumor cells to the blood vessels, from where they can disseminate throughout the body.

Tumor cell-driven extracellular matrix remodeling enables haptotaxis during metastatic progression

Madeleine J. Oudin1Oliver Jonas1Tatsiana Kosciuk1Liliane C. Broye1Bruna C. Guido1Jeff Wyckoff1, …., James E. Bear2 and Frank B. Gertler1,*
Cancer Discov CD-15-1183  Jan 25, 2016  http://dx.doi.org:/10.1158/2159-8290.CD-15-1183

Fibronectin (FN) is a major component of the tumor microenvironment, but its role in promoting metastasis is incompletely understood. Here we show that FN gradients elicit directional movement of breast cancer cells, in vitro and in vivo. Haptotaxis on FN gradients requires direct interaction between α5β1 integrin and Mena, an actin regulator, and involves increases in focal complex signaling and tumor-cell-mediated extracellular matrix (ECM) remodeling. Compared to Mena, higher levels of the pro-metastatic MenaINV isoform associate with α5, which enables 3D haptotaxis of tumor cells towards the high FN concentrations typically present in perivascular space and in the periphery of breast tumor tissue. MenaINV and FN levels were correlated in two breast cancer cohorts, and high levels of MenaINV were significantly associated with increased tumor recurrence as well as decreased patient survival. Our results identify a novel tumor-cell-intrinsic mechanism that promotes metastasis through ECM remodeling and ECM guided directional migration.

 

Researchers Find Link Between Death of Tumor-support Cells and Cancer Metastasis       Fri, 02/19/2016
http://www.dddmag.com/news/2016/02/researchers-find-link-between-death-tumor-support-cells-and-cancer-metastasis#.VuatbTol_kI.linkedin

The images show tumors that have metastasized to the lungs (image b) and bones (image d) in mice that had CAFs eliminated after 10 days. (Credit: Biju Parekkadan, Massachusetts General Hospital)

http://www.dddmag.com/sites/dddmag.com/files/20160219-metastasized-cells%20%281%29.jpg

The images show tumors that have metastasized to the lungs (image b) and bones (image d) in mice that had CAFs eliminated after 10 days. (Credit: Biju Parekkadan, Massachusetts General Hospital)

Researchers have discovered that eliminating cells thought to aid tumor growth did not slow or halt the growth of cancer tumors. In fact, when the cancer-associated fibroblasts (CAFs), were eliminated after 10 days, the risk of metastasis of the primary tumor to the lungs and bones of mice increased dramatically. Scientists used bioengineered CAFs equipped with genes that caused those cells to self-destruct at defined moments in tumor progression. The study, published in Scientific Reports on Feb. 19, was conducted by researchers funded by the National Institute of Biomedical Imaging and Bioengineering (NIBIB) at Massachusetts General Hospital (MGH). NIBIB is part of the National Institutes of Health.

What causes cancer to grow and metastasize is not well understood by scientists. CAFs are thought to be fibroblast cells native to the body that cancer cells hijacks and use to sustain their growth. However, because fibroblasts are found throughout the human body, it can be difficult to follow and study cancer effects on these cells.

“This work underscores two important things in solving the puzzle that is cancer,” said Rosemarie Hunziker, Ph.D., program director for Tissue Engineering at NIBIB. “First, we are dealing with a complex disease with so many dimensions that we are really only just beginning to describe it.  Second, this approach shows the power of cell engineering — manipulating a key cell in the cancer environment has led to a significant new understanding of how cancer grows and how it might be controlled in the future.”

Biju Parekkadan, Ph.D., assistant professor of surgery and bioengineering at MGH, and his team designed an experiment with the goal of better understanding the cellular environment in which tumors exist (called tumor microenvironment or TME), and the role of CAFs in tumor growth. In an effort to understand whether targeting CAFs could limit the growth of breast cancer tumors implanted in mice, they bioengineered CAFs with a genetic “kill switch.” The cells were designed to die when exposed to a compound that was not toxic to the surrounding cells.

Parekkadan and his team chose two different stages of tumor growth in which the CAFs were killed off after the tumor was implanted. When the CAFs were eliminated on the third or fourth day, they found no major difference in tumor growth or risk of metastasis compared with the tumors where the CAFs remained. However, there was an increase in tumor-associated macrophages — cells that have been associated with metastasis — in this early stage.

When the team waited to eliminate the CAFs until the 10th or 11th day, they discovered that in addition to the increase in macrophages, the cancer was more likely to spread to the lungs and bones of the mice. The unexpected results from this experiment could spur more research into the role of CAFs in cancer growth and metastasis.

More research may reveal whether or not there is a scientific basis for targeting CAFs for destruction — and if so, the awareness that timing matters when it comes to the response of the tumor. While neither treatment affected the growth of the initial tumor, it is important to understand that most cancer deaths result from metastases to vital organs rather than from the direct effects of the primary tumor.

 

 

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Dopamine-β-Hydroxylase Functional Variants

Curator: Larry H. Bernstein, MD, FCAP

 

 

Deep sequencing identifies novel regulatory variants in the distal promoter region of the dopamine-β-hydroxylase gene.

OBJECTIVE:

Dopamine-β-hydroxylase (DBH), an enzyme that converts dopamine into norepinephrine, is a drug target in cardiovascular and neuropsychiatric disorders. We aimed to identify functional variants in this gene by deep sequencing and enzyme phenotyping in an Indian cohort.

MATERIALS AND METHODS:

Targeted resequencing of 12 exons and 10 kb upstream sequences of DBH in healthy volunteers (n=50) was performed using the Ion Personal Genome Machine System. Enzyme quantity and activity in their sera samples were determined by ELISA and ultra performance liquid chromatography, respectively. The association of markers with phenotypes was determined using Matrix eQTL. Global P-values for haplotypes generated using UNPHASED 3.1.5 were graphed using GrASP v.082 beta.

RESULTS:

Of the 49 variants identified, nine were novel (minor allele frequency≥0.01). Though individual markers associated with enzyme quantity did not withstand multiple corrections, a novel distal promoter block driven by rs113249250 (global P=1.5×10) was associated. Of the nine single nucleotide polymorphisms (SNPs) associated with enzyme activity, rs3025369, rs1076151 and rs1611115, all from the upstream region, withstood false discovery rate correction (false discovery rate=0.03, 0.03 and 2.9×10, respectively). Conditioning for rs1611115 identified rs1989787 also to affect activity. Importantly, we report an association of a novel haplotype block distal to rs1076151 driven by rs3025369 (global P=8.9×10) with enzyme activity. This regulatory SNP explained 4.9% of the total 46.1% of variance in DBH activity caused by associated SNPs.

CONCLUSION:

This first study combining deep sequencing and enzyme phenotyping identified yet another regulatory SNP suggesting that regulatory variants may be central in the physiological or metabolic role of this gene of therapeutic and pharmacological relevance.

 

 

Correlation of plasma dopamine beta-hydroxylase activity with polymorphisms in DBH gene: a study on Eastern Indian population.

Plasma dopamine beta-hydroxylase activity (plDbetaH) is tightly regulated by the DBH gene and several genetic polymorphisms have been found to independently exert their influence. In the present investigation, association of four DBH polymorphisms, DBH-STR, rs1611115, rs1108580, and rs2519152 with plDbetaH was examined in blood samples from 100 unrelated individuals belonging to the state of West Bengal, Eastern India. Genotypes obtained after PCR amplification and restriction digestion were used for statistical analyses. plDbetaH was measured using a photometric assay and its correlation with the genetic polymorphisms was analyzed using analysis of variance and linear regression. Moderate linkage disequilibrium (LD) was observed between DBH-STR and rs1611115, while rs1108580 and rs2519152 were in strong LD. ‘T’ allele of rs1611115 showed strong negative correlation with plDbetaH, whereas DBH-STR, rs1108580 and rs2519152 had no major effect. Four haplotypes showed significant influence on plDbetaH. This is the first report on the effect of genetic polymorphisms on plDbetaH from the Indian sub-continent. rs1611115 was the only polymorphism that showed substantial control over plDbetaH. Other polymorphisms which did not show individual effects could possibly be part of larger haplotype blocks that carry the functional polymorphisms controlling plDbetaH.
Polymorphisms and low plasma activity of dopamine-beta-hydroxylase in ADHD children.
Attention-deficit Hyperactivity disorder (ADHD) is a multifactorial disorder clinically characterized by inattentiveness, impulsivity and hyperactivity. The occurrence of this disorder is between 3 and 6% of the children population, with boys predominating over girls at a ratio of 3:1 or more. The research of some candidate genes (DRD4, DAT, DRD5, DBH, 5HTT, HTR1B and SNAP25) brought consistent results confirming the heredity of ADHD syndromes. Dopamine-beta-hydroxylase (DBH) is an enzyme responsible for the conversion of dopamine into noradrenaline. Alteration of the dopamine/noradrenaline levels can result in hyperactivity. The DBH protein is released in response to stimulation. DBH activity, derived largely from sympathetic nerves, can be measured in human plasma. Patients with ADHD showed decreased activities of DBH in serum and urine. Low DBH levels correlate indirectly with the seriousness of the hyperkinetic syndrome in children [19,20]. In the DBH gene, the G444A, G910T, C1603T, C1912T, C-1021T, 5 -ins/del and TaqI polymorphisms occur frequently and may affect the function of gene products or modify gene expression and thus influence the progression of ADHD. This article reviews the DBH itself and polymorphisms in the DBH gene that influence the DBH activity in the serum and the CSF level of DBH. All those are evaluated in connection with ADHD.
Candidate gene studies of attention-deficit/hyperactivity disorder.
A growing body of behavioral and molecular genetics literature has indicated that the development of attention-deficit/hyperactivity disorder (ADHD) may be attributed to both genetic and environmental factors. Family, twin, and adoption studies provide compelling evidence that genes play a strong role in mediating susceptibility to ADHD. Molecular genetic studies suggest that the genetic architecture of ADHD is complex, while the handful of genome-wide scans conducted thus far is not conclusive. In contrast, the many candidate gene studies of ADHD have produced substantial evidence implicating several genes in the etiology of the disorder. For the 8 genes for which the same variant has been studied in 3 or more case-control or family-based studies, 7 show statistically significant evidence of association with ADHD based on pooled odds ratios across studies: the dopamine D4 receptor gene (DRD4), the dopamine D5 receptor gene (DRD5), the dopamine transporter gene (DAT), the dopamine beta-hydroxylase gene (DBH), the serotonin transporter gene (5-HTT), the serotonin receptor 1B gene (HTR1B), and the synaptosomal-associated protein 25 gene (SNAP25). Recent pharmacogenetic studies have correlated treatment nonresponse with particular gene markers, while preclinical studies have increased our understanding of gene expression paradigms and potential analogs for human trials. This literature review discusses the relevance and implications of genetic associations with ADHD for clinical practice and future research
Lack of significant association between -1021C–>T polymorphism in the dopamine beta hydroxylase gene and attention deficit hyperactivity disorder.
Recent trends in medications for attention deficit hyperactivity disorder (ADHD) suggest that norepinephrine (NE) deficiency may contribute to the disease etiology. Dopamine beta hydroxylase (DBH) is the key enzyme which converts dopamine to NE and since DBH gene is considered a major quantitative trait locus for plasma DBH activity, genetic polymorphism may lead to altered NE neurotransmission. Several polymorphisms including a 5′ flanking -1021C–>T polymorphism, was reported to be associated with changed DBH activity and an association between -1021C–>T polymorphism with ADHD was observed in Han Chinese children. We have carried out family-based studies with three polymorphisms in the DBH gene, -1021C–>T polymorphism, exon 2*444g/a and intron 5 TaqI RFLP, to explore their association with Indian ADHD cases. Allele and genotype frequency of these polymorphisms in ADHD cases were compared with that of their parents and a control group. Haplotypes obtained were analyzed for linkage disequilibrium (LD). Haplotype-based haplotype relative risk analysis and transmission disequilibrium test showed lack of significant association between transmission of the polymorphisms and ADHD. A haplotype comprising of allele 1 of all polymorphisms showed a slight positive trend towards transmission from parents to ADHD probands. Strong LD was observed between *444g/a and TaqI RFLP in all the groups. However, low D’ values and corresponding log of odds scores in the control group as compared to the ADHD families indicated that, the incidence of the two polymorphisms being transmitted together could be higher in ADHD families.
Association of the dopamine beta hydroxylase gene with attention deficit hyperactivity disorder: genetic analysis of the Milwaukee longitudinal study.
Attention deficit hyperactivity disorder (ADHD) is a highly heritable and common disorder that partly reflects disturbed dopaminergic function in the brain. Recent genetic studies have shown that candidate genes involved in dopamine signaling and metabolism contribute to ADHD susceptibility. We have initiated genetic studies in a unique cohort of 158 ADHD and 81 control adult subjects who have been followed longitudinally since childhood in the Milwaukee study of ADHD. From this cohort, genetic analysis was performed in 105 Caucasian subjects with ADHD and 68 age and ethnicity-matched controls for the DRD4 exon 3 VNTR, the SLC6A3 (DAT1) 3′ UTR VNTR, dopamine beta hydroxylase (DBH) TaqI A polymorphism, and the DBH GT microsatellite repeat polymorphism that has been quantitatively associated with serum levels of DBH activity, but not previously studied in ADHD. Results indicate a significant association between the DBH TaqI A1 allele and ADHD (P = 0.018) with a relative risk of 1.33. The DBH GT repeat 4 allele, which is associated with high serum levels of DBH, occurred more frequently in the ADHD group than controls, but the difference did not reach statistical significance. Associations were not found with the SLC6A3 10 repeat or DRD4 7 repeat alleles. These results indicate that the DBH TaqI A allele, or another polymorphism in linkage disequilibrium with this allele, may confer increased susceptibility towards ADHD.
Polymorphisms of the dopamine transporter gene: influence on response to methylphenidate in attention deficit-hyperactivity disorder.
Attention deficit-hyperactivity disorder (ADHD) is a very common and heterogeneous childhood-onset psychiatric disorder, affecting between 3% and 5% of school age children worldwide. Although the neurobiology of ADHD is not completely understood, imbalances in both dopaminergic and noradrenergic systems have been implicated in the origin and persistence of core symptoms, which include inattention, hyperactivity, and impulsivity. The role of a genetic component in its etiology is strongly supported by genetic studies, and several investigations have suggested that the dopamine transporter gene (DAT1; SLC6A3 locus) may be a small-effect susceptibility gene for ADHD. Stimulant medication has a well-documented efficacy in reducing ADHD symptoms. Methylphenidate, the most prescribed stimulant, seems to act mainly by inhibiting the dopamine transporter protein and dopamine reuptake. In fact, its effect is probably related to an increase in extracellular levels of dopamine, especially in brain regions enriched in this protein (i.e. striatum). It is also important to note that dopamine transporter densities seem to be particularly elevated in the brain of ADHD patients, decreasing after treatment with methylphenidate. Altogether, these observations suggest that the dopamine transporter does play a major role in ADHD. Among the several polymorphisms already described in the SLC6A3 locus, a 40 bp variable number of tandem repeats (VNTR) polymorphism has been extensively investigated in association studies with ADHD. Although there are some negative results, the findings from these reports indicate the allele with ten copies of the 40 bp sequence (10-repeat allele) as the risk allele for ADHD. Some investigations have suggested that this polymorphism can be implicated in dopamine transporter gene expression in vitro and dopamine transporter density in vivo, even though it is located in a non-coding region of the SLC6A3 locus. Despite all these data, few studies have addressed the relationship between genetic markers (specifically the VNTR) at the SLC6A3 locus and response to methylphenidate in ADHD patients. A significant effect of the 40 bp VNTR on response to methylphenidate has been detected in most of these reports. However, the findings are inconsistent regarding both the allele (or genotype) involved and the direction of this influence (better or worse response). Thus, further investigations are required to determine if genetic variation due to the VNTR in the dopamine transporter gene is able to predict different levels of clinical response and palatability to methylphenidate in patients with ADHD, and how this information would be useful in clinical practice.
Pharmacogenomics in psychiatry: the relevance of receptor and transporter polymorphisms.
The treatment of severe mental illness, and of psychiatric disorders in general, is limited in its efficacy and tolerability. There appear to be substantial interindividual differences in response to psychiatric drug treatments that are generally far greater than the differences between individual drugs; likewise, the occurrence of adverse effects also varies profoundly between individuals. These differences are thought to reflect, at least in part, genetic variability. The action of psychiatric drugs primarily involves effects on synaptic neurotransmission; the genes for neurotransmitter receptors and transporters have provided strong candidates in pharmacogenetic research in psychiatry. This paper reviews some aspects of the pharmacogenetics of neurotransmitter receptors and transporters in the treatment of psychiatric disorders. A focus on serotonin, catecholamines and amino acid transmitter systems reflects the direction of research efforts, while relevant results from some genome-wide association studies are also presented. There are many inconsistencies, particularly between candidate gene and genome-wide association studies. However, some consistency is seen in candidate gene studies supporting established pharmacological mechanisms of antipsychotic and antidepressant response with associations of functional genetic polymorphisms in, respectively, the dopamine D2 receptor and serotonin transporter and receptors. More recently identified effects of genes related to amino acid neurotransmission on the outcome of treatment of schizophrenia, bipolar illness or depression reflect the growing understanding of the roles of glutamate and γ-aminobutyric acid dysfunction in severe mental illness. A complete understanding of psychiatric pharmacogenomics will also need to take into account epigenetic factors, such as DNA methylation, that influence individual responses to drugs.
Pharmacogenetics of psychotropic drug response.

OBJECTIVE:

Molecular genetic approaches provide a novel method of dissecting the heterogeneity of psychotropic drug response. These pharmacogenetic strategies offer the prospect of identifying biological predictors of psychotropic drug response and could provide the means of determining the molecular substrates of drug efficacy and drug-induced adverse events.

METHOD:

The authors discuss methods issues in executing pharmacogenetic studies, review the first generation of pharmacogenetic studies of psychotropic drug response, and consider future directions for this rapidly evolving field.

RESULTS:

Pharmacogenetics has been most commonly used in studies of antipsychotic drug efficacy, antidepressant drug response, and drug-induced adverse effects. Data from antipsychotic drug studies indicate that polymorphisms within the serotonin 2A and dopamine receptor 2 genes may influence drug efficacy in schizophrenia. Moreover, a growing body of data suggests a relationship between the serotonin transporter gene and clinical effects of the selective serotonin reuptake inhibitors used to treat depression. A significant relationship between genetic variation in the cytochrome P450 system and drug-induced adverse effects may exist for certain medications. Finally, a number of independent studies point to a significant effect of a dopamine D(3) receptor polymorphism on susceptibility to tardive dyskinesia.

CONCLUSIONS:

Initial research into the pharmacogenetics of psychotropic drug response suggests that specific genes may influence phenotypes associated with psychotropic drug administration. These results remain preliminary and will require further replication and validation. New developments in molecular biology, human genomic information, statistical methods, and bioinformatics are ongoing and could pave the way for the next generation of pharmacogenetic studies in psychiatry.

OBJECTIVE: Molecular genetic approaches provide a novel method of dissecting the heterogeneity of psychotropic drug response. These pharmacogenetic strategies offer the prospect of identifying biological predictors of psychotropic drug response and could provide the means of determining the molecular substrates of drug efficacy and drug-induced adverse events. METHOD: The authors discuss methods issues in executing pharmacogenetic studies, review the first generation of pharmacogenetic studies of psychotropic drug response, and consider future directions for this rapidly evolving field. RESULTS: Pharmacogenetics has been most commonly used in studies of antipsychotic drug efficacy, antidepressant drug response, and drug-induced adverse effects. Data from antipsychotic drug studies indicate that polymorphisms within the serotonin 2A and dopamine receptor 2 genes may influence drug efficacy in schizophrenia. Moreover, a growing body of data suggests a relationship between the serotonin transporter gene and clinical effects of the selective serotonin reuptake inhibitors used to treat depression. A significant relationship between genetic variation in the cytochrome P450 system and drug-induced adverse effects may exist for certain medications. Finally, a number of independent studies point to a significant effect of a dopamine D3 receptor polymorphism on susceptibility to tardive dyskinesia. CONCLUSIONS: Initial research into the pharmacogenetics of psychotropic drug response suggests that specific genes may influence phenotypes associated with psychotropic drug administration. These results remain preliminary and will require further replication and validation. New developments in molecular biology, human genomic information, statistical methods, and bioinformatics are ongoing and could pave the way for the next generation of pharmacogenetic studies in psychiatry.

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Tracking protein expression

Larry H. Bernstein, MD, FCAP, Curator

LPBI

 

Protein Counting in Single Cancer Cells

Stephanie M. Schubert, Stephanie R. Walter, Mael Manesse, and David R. Walt*
Analytical Chemistry  Anal. Chem., 2016, 88 (5), pp 2952–2957   http://dx.doi.org:/10.1021/acs.analchem.6b00146

 

Abstract Image

 

 

The cell is the basic unit of biology and protein expression drives cellular function. Tracking protein expression in single cells enables the study of cellular pathways and behavior, but requires methodologies sensitive enough to detect low numbers of protein molecules with a wide dynamic range to distinguish unique cells and quantify population distributions. This study presents an ultrasensitive and automated approach for quantifying phenotypic responses with single cell resolution using single molecule array (Simoa) technology. We demonstrate how prostate specific antigen (PSA) expression varies over several orders of magnitude between single prostate cancer cells, and how PSA expression shifts with genetic drift. Single cell Simoa intduces a straightforward process that is capable of detecting both high and low protein expression levels. This technique could be useful for understanding fundamental biology and may eventually enable both earlier disease detection and targeted therapy.

 

Quanterix’s proprietary Simoa™ technology (named for single molecule array) is based upon the isolation of individual immunocomplexes on paramagnetic beads using standard ELISA reagents. The main difference between Simoa and conventional immunoassays lies in the ability to trap single molecules in femtoliter-sized wells, allowing for a “digital” readout of each individual bead to determine if it is bound to the target analyte or not.

The digital nature of the technique allows an average of 1000x sensitivity increase over conventional assays with CVs <10%.

 

 

A. Single protein molecules are captured and labeled on beads using standard ELISA reagents.

 

B. Tens of thousands of beads – with or without immunoconjugate – are mixed with enzyme substrate and loaded into individual femtoliter-sized wells.

 

C. The microwells are sealed with oil.

 

D. Fluorophore concentration in the small sample volume of wells containing the target analyte rapidly reach detectable limits using conventional fluorescence imaging and can be digitally counted.

E. The percentage of beads containing labelled immunocomplexes can be computed at low concentration because they follow a Poisson distribution; at higher concentrations the intensity of the aggregate signal provides an analog measurement.

 

 

Clin Chem Lab Med. 2015 Oct 23. pii: /j/cclm.ahead-of-print/cclm-2015-0733/cclm-2015-0733.xml. http://dx.doi.org:/10.1515/cclm-2015-0733. [Epub ahead of print]
Assessing the commutability of reference material formats for the harmonization of amyloid beta measurements.

The cerebrospinal fluid (CSF) amyloid-β (Aβ42) peptide is an important biomarker for Alzheimer’s disease (AD). Variability in measured Aβ42 concentrations at different laboratories may be overcome by standardization and establishing traceability to a reference system. Candidate certified reference materials (CRMs) are validated herein for this purpose.

METHODS:

Commutability of 16 candidate CRM formats was assessed across five CSF Aβ42 immunoassays and one mass spectrometry (MS) method in a set of 48 individual clinical CSF samples. Promising candidate CRM formats (neat CSF and CSF spiked with Aβ42) were identified and subjected to validation across eight (Elecsys, EUROIMMUN, IBL, INNO-BIA AlzBio3, INNOTEST, MSD, Simoa, and Saladax) immunoassays and the MS method in 32 individual CSF samples. Commutability was evaluated by Passing-Bablok regression and the candidate CRM termed commutable when found within the prediction interval (PI). The relative distance to the regression line was assessed.

RESULTS:

The neat CSF candidate CRM format was commutable for almost all method comparisons, except for the Simoa/MSD, Simoa/MS and MS/IBL where it was found just outside the 95% PI. However, the neat CSF was found within 5% relative distance to the regression line for MS/IBL, between 5% and 10% for Simoa/MS and between 10% and 15% for Simoa/MSD comparisons.

CONCLUSIONS:

The neat CSF candidate CRM format was commutable for 33 of 36 method comparisons, only one comparison more than expected given the 95% PI acceptance limit. We conclude that the neat CSF candidate CRM can be used for value assignment of the kit calibrators for the different Aβ42 methods.

 

 

Nature Neuroscience18, 1559–1561(2015)    http://dx.doi.org:/10.1038/nn.4117

Cerebral β-amyloidosis is induced by inoculation of Aβ seeds into APP transgenic mice, but not into App−/− (APP null) mice. We found that brain extracts from APP null mice that had been inoculated with Aβ seeds up to 6 months previously still induced β-amyloidosis in APP transgenic hosts following secondary transmission. Thus, Aβ seeds can persist in the brain for months, and they regain propagative and pathogenic activity in the presence of host Aβ.

 

Induced amyloid lesions are partly congophilic and surrounded by activated microglia and dystrophic boutons.

Induced amyloid lesions are partly congophilic and surrounded by activated microglia and dystrophic boutons.

(a) Congo red-positive amyloid deposits induced in the dentate gyrus were surrounded by Iba1-positive microglia (black). (b) Congo red-positive plaque with surrounding hypertrophic microglial cell bodies and processes at higher magnification

 

Glial fibrillary acidic protein is a body fluid biomarker for glial pathology in human disease

Brain Research  Volume 1600, 10 March 2015, Pages 17–31    doi:10.1016/j.brainres.2014.12.027

Highlights

• Reviewing 45 years of Glial fibrillary acidic protein (Gfap).
•Gfap discovered in multiple sclerosis brain tissue.
•From Gfap genetics to post-translational modifications.
•Ninety-nine ways to quantify Gfap and related immune phenomena.
•Emergence of Gfap as a body fluid biomarker in human disease.

This review on the role of glial fibrillary acidic protein (GFAP) as a biomarker for astroglial pathology in neurological diseases provides background to protein synthesis, assembly, function and degeneration. Qualitative and quantitative analytical techniques for the investigation of human tissue and biological fluid samples are discussed including partial lack of parallelism and multiplexing capabilities. Pathological implications are reviewed in view of immunocytochemical, cell-culture and genetic findings. Particular emphasis is given to neurodegeneration related to autoimmune astrocytopathies and to genetic gain of function mutations. The current literature on body fluid levels of GFAP in human disease is summarised and illustrated by disease specific meta-analyses. In addition to the role of GFAP as a diagnostic biomarker for chronic disease, there are important data on the prognostic value for acute conditions. The published evidence permits to classify the dominant GFAP signatures in biological fluids. This classification may serve as a template for supporting diagnostic criteria of autoimmune astrocytopathies, monitoring disease progression in toxic gain of function mutations, clinical treatment trials (secondary outcome and toxicity biomarker) and provide prognostic information in neurocritical care if used within well defined time-frames.

 

The GFAP isoforms. A schematic drawing of the protein structures of the GFAP ...

 

Modelled structure of GFAP. Reprinted with permission from Biswas et al. (2011).

 

CSF and Plasma Amyloid-b Temporal Profiles and Relationships with Neurological Status and Mortality after Severe Traumatic Brain Injury

http://www.quanterix.com/literature/publications/neurology/item/482-csf-and-plasma-amyloid-b-temporal-profiles-and-relationships-with-neurological-status-and-mortality-after-severe-traumatic-brain-injury

by Stefania Mondello, Andras Burk, Pal Barzo, Jeff Randall, Gail Provuncher, David Hanlon, David Wilson, Firas Kobeissy & Andreas Jeromin

 

The role of amyloid-b (Ab) neuropathology and its significant changes in biofluids after traumatic braininjury (TBI) is still debated. We used ultrasensitive digital  ELISA approach to assess amyloid-b1-42 (Ab42) concentrations and time-course in cerebrospinal fluid (CSF) and in plasma of patients with severe TBI and
investigated their relationship to injury characteristics, neurological status and clinical outcome. We found decreased CSF Ab42 levels in TBI patients acutely after injury with lower levels in patients who died 6 months post-injury than in survivors. Conversely, plasma Ab42 levels were significantly increased in TBI
with lower levels in patients who survived. A trend analysis showed that both CSF and plasma Ab42 levels strongly correlated with mortality. A positive correlation between changes in CSF Ab42 concentrations and neurological status as assessed by Glasgow Coma Scale (GCS) was identified. Our results suggest that determination of Ab42 may be valuable to obtain prognostic information in patients with severe TBI as well as in monitoring the response of the brain to injury.
Plasma tau levels in Alzheimer’s disease
Henrik Zetterberg, David Wilson, Ulf Andreasson, Lennart Minthon, Kaj Blennow, Jeffrey Randall and Oskar Hansson
Alzheimer’s Research & Therapy 2013; 5:9   http://dx.doi.org:/10.1186/alzrt163

Efforts to find reliable blood biomarkers for Alzheimer’s disease (AD) in a highly warranted clinical laboratory test have met with little success. There is no clear change in plasma β-amyloid in AD, and assays for the axonal injury marker tau have been hampered by a lack of analytical sensitivity for accurate measurement in blood samples [1]. Here, the results of a novel ultra-sensitive assay for tau in peripheral blood are reported.

We have developed an ultra-sensitive assay for tau in peripheral blood [2]. In brief, the assay is based on digital array technology [3] and uses the Tau5 monoclonal antibody for capture (Covance, Princeton, NJ, USA) and HT7 and BT2 monoclonal antibodies for detection (Pierce, now part of Thermo Fisher Scientific Inc., Waltham, MA, USA). This combination reacts with both normal and phosphorylated tau with epitopes in the mid-region of the molecule, making the assay sensitive to all known tau isoforms. The calibrator was recombinant tau 381 (EMD Millipore Corporation, Billerica, MA, USA). To minimize matrix effects, all samples were diluted 1:4 in phosphate-buffered saline with 2% bovine serum albumin diluent prior to assay. The limit of detection of the assay, which requires 30 μL of plasma, is 0.02 pg/mL [2], which is more than 1,000-fold more sensitive than conventional immunoassays.

Here, we assess the association of plasma tau levels with AD in a cross-sectional study of 54 patients with AD dementia [4], 75 patients with mild cognitive impairment (MCI) [5], and 25 cognitively normal controls (Table 1). All participants were recruited at the specialized memory clinic at Skåne University Hospital in Malmö, Sweden, and underwent extensive clinical evaluation, including cerebrospinal fluid (CSF) sampling by lumbar puncture, in addition to venipuncture and collection of blood in ethylenediaminetetraacetic acid (EDTA) tubes for plasma preparation by centrifugation within 15 minutes from sampling. Plasma samples were aliquoted into cryo tubes and stored at -80°C pending analysis, which was performed on one occasion by using one batch of reagents with an average coefficient of variation of 9.7% for triplicate measurements of each sample. The patients with MCI were cognitively stable for an average of 101 months (n = 36) or developed AD dementia (n = 35) or other types of dementias – vascular dementia (n = 3) and semantic dementia (n = 1) – during follow-up. The study was approved by the regional ethics committee at Lund University and complied with the Declaration of Helsinki. Informed consent was obtained from all study participants.
Tau levels in plasma were significantly higher in AD patients compared with both controls and MCI patients (Figure 1a). MCI patients who developed AD during follow-up had tau levels similar to those of patients with stable MCI and cognitively normal controls (Figure 1b). There was no correlation between tau levels in plasma and CSF in any diagnostic group (Figure 1c).
https://static-content.springer.com/image/art%3A10.1186%2Falzrt163/MediaObjects/13195_2013_Article_139_Fig1_HTML.jpg

Figure 1

Elevated tau levels in plasma from patients with Alzheimer’s disease (AD). (a) Plasma levels of tau are elevated in patients with AD compared with cognitively normal controls and patients with mild cognitive impairment (MCI). (b) MCI patients who developed AD (MCI-AD) during follow-up had baseline tau levels similar to those of patients with stable MCI (SMCI). (c) There was no correlation between tau levels in plasma and cerebrospinal fluid (CSF) in any diagnostic group. Thin horizontal lines in panels (a) and (b) indicate medians. A nonparametric Kruskal-Wallis test followed by Mann-Whitney was performed to test for statistical significance. Spearman’s rank correlation coefficient was used to assess the relationship between plasma and CSF tau concentrations in panel (c), where open circles, gray squares, and black triangles represent AD, MCI, and controls, respectively.

The results of this study have several important implications. First, plasma tau levels are elevated in AD but with overlapping ranges across diagnostic groups. This overlap diminishes the utility of plasma tau as a diagnostic test. However, further studies are needed to evaluate plasma tau as a first-in-line screening tool (for example, in the primary care setting and perhaps together with other markers in a biomarker panel). Second, normal plasma tau levels in the MCI stage of AD suggest that plasma tau is a late marker, requiring substantial axonal injury before increasing to abnormal levels. In this context, other neurodegenerative diseases (for example, Creutzfeldt-Jakob disease) as well as acute conditions (for example, stroke and brain trauma) should be tested. Third, the lack of correlation of tau levels in plasma and CSF suggests that steady-state concentrations of tau in these two body fluids are differentially regulated. In our earlier study of patients with hypoxic brain injury following cardiac arrest, tau was rapidly (within 24 hours) cleared from blood in patients with good neurological outcome [2], indicating potent clearance mechanisms for this marker in the bloodstream. This may obscure any correlation with CSF tau levels, which stay elevated for weeks following an acute neurological insult [6].

Researchers Use CRISPR-based Method to Track RNA In Vivo

A research team led by researchers from the University of California has modified the CRISPR/Cas9 system to demonstrate the ability to track specific RNA sequences and processes in vivo.

As described in a paper published today in Cell, the investigators were able to use their system to visualize specific RNA molecules accumulating in stress granules — dense aggregations of proteins and RNA that form in the cytosol in response to cellular stress and have been linked to neurodegenerative disorders such as amyotrophic lateral sclerosis.

They also found that they could use Cas9 to target an mRNA without altering mRNA abundance or the amount of translated protein.

“We are just beginning to see the implications of genome engineering using the CRISPR technology, but many diseases, including cancer and autism, are linked to problems with another fundamental biological molecule: RNA,” Gene Yeo, senior study author and an associate professor at the University of California, San Diego, said in a statement.

The researchers began their project based on a modification attempted in the lab of co-author Jennifer Doudna from the University of California, Berkeley. Inthat study, the researchers found that it was possible to design a protospacer adjacent motif (PAM) as part of an oligonucleotide (PAMmer) which binds to the single-stranded RNA, allowing Cas9 to efficiently recognize and cleave RNA rather than DNA (RCas9). The researchers determined that with a few further modifications, they could use this method to not only recognize RNA instead of DNA but actually track its movements through cells.

Previously, researchers have attempted to use molecular beacons to track RNA sequences, however, these are limited to imaging applications and are difficult to deliver into cells. Researchers have also attempted to use aptamers to enable RNA tracking in living cells, but these are limited in the number of RNA sequences that they can recognize.

CRISPR/Cas9, however, has thus far proved extremely useful in the genome engineering field and the research team thought that it would be an ideal base to create a better RNA tracking tool.

To prove their concept, the team tested whether a dead Cas9 (dCas9) that was tagged with the fluorescent protein mCherry and contained a nuclear localization signal could be co-exported from the nucleus with a messenger RNA in the presence of a single-guide RNA (sgRNA) and PAMmer designed to recognize that specific mRNA.

The experiment succeeded and the researchers were also able to observe accumulation of ACTB, CCNA2, and TFRC mRNAs in RNA granules that correlated with fluorescence in situ hybridization visualization using image analysis software.

Once they had established that their method was effective, the researchers showed that they could use the sgRNA and PAMmer targeting sequences to track mRNA trafficking to stress granules.

The researchers demonstrated that they could take time-resolved measurements of ACTB mRNA trafficking to stress granules over a period of 30 minutes. They noted in the paper that RCas9 was capable of measuring the association of CCNA2 and TFRC mRNA trafficking to stress granules, as well.

Based on their results, the investigators believe they have established RCas9 as a means to track RNA in living cells in a programmable manner that doesn’t require genetically encoded tags.

“One potential application of this technique is to track RNA transport in diseased neurons over time in order to identify the molecular features of these diseases and support the developments of therapies,” David Nelles, first author on the study and a researcher at the University of California, San Diego, said in a statement. “Just as CRISPR-Cas9 is making genetic engineering accessible to any scientists with access to basic equipment, RNA-targeted Cas9 may support countless other efforts for studying the role of RNA processing in disease or for identifying drugs that reverse defects in RNA processing.”

 

Programmable RNA Tracking in Live Cells with CRISPR/Cas9

David A. Nelles, Mark Y. Fang, Mitchell R. O’Connell, Jia L. Xu, Sebastian J. Markmiller, Jennifer A. Doudna, Gene W. Yeo
Publication stage: In Press Corrected Proof
Figure thumbnail fx1

Clustered regularly-interspaced short palindromic repeats (CRISPRs) form the basis of adaptive immune systems in bacteria and archaea by encoding CRISPR RNAs that guide CRISPR-associated (Cas) nucleases to invading genetic material (Wiedenheft et al., 2012). Cas9 from the type II CRISPR system ofS. pyogenes has been repurposed for genome engineering in eukaryotic organisms (Hwang et al., 2013, Li et al., 2013a, Mali et al., 2013, Nakayama et al., 2013, Sander and Joung, 2014, Yang et al., 2014) and is rapidly proving to be an efficient means of DNA targeting for other applications such as gene expression modulation (Qi et al., 2013) and imaging (Chen et al., 2013). Cas9 and its associated single-guide RNA (sgRNA) require two critical features to target DNA: a short DNA sequence of the form 5′-NGG-3′ (where “N” = any nucleotide) known as the protospacer adjacent motif (PAM) and an adjacent sequence on the opposite DNA strand that is antisense to the sgRNA. By supporting DNA recognition with specificity determined entirely by a short spacer sequence within the sgRNA, CRISPR/Cas9 provides uniquely flexible and accessible manipulation of the genome. Manipulating cellular RNA content, in contrast, remains problematic. Whereas there exist robust means of attenuating gene expression via RNAi and antisense oligonucleotides, other critical aspects of post-transcriptional gene expression regulation such as subcellular trafficking, alternative splicing or polyadenylation, and spatiotemporally restricted translation are difficult to measure in living cells and are largely intractable.

Analogous to the assembly of zinc finger nucleases (Urnov et al., 2010) and transcription activator-like effector nucleases (TALEN) to recognize specific DNA sequences, efforts to recognize specific RNA sequences have focused on engineered RNA-binding domains. Pumilio and FBF homology (PUF) proteins carry well-defined modules capable of recognizing a single base each and have supported successful targeting of a handful of transcripts for imaging and other manipulations (Filipovska et al., 2011, Ozawa et al., 2007, Wang et al., 2009). PUF proteins can be fused to arbitrary effector domains to alter or tag target RNAs, but PUFs must be redesigned and validated for each RNA target and can only recognize eight contiguous bases, which does not allow unique discrimination in the transcriptome. Molecular beacons are self-quenched synthetic oligonucleotides that fluoresce upon binding to target RNAs and allow RNA detection without construction of a target-specific protein (Sokol et al., 1998). But molecular beacons must be microinjected to avoid the generation of excessive background signal associated with endosome-trapped probes and are limited to imaging applications. An alternative approach to recognition of RNA substrates is to introduce RNA aptamers into target RNAs, enabling specific and strong association of cognate aptamer-binding proteins such as the MS2 coat protein (Fouts et al., 1997). This approach has enabled tracking of RNA localization in living cells over time with high sensitivity (Bertrand et al., 1998) but relies upon laborious genetic manipulation of the target RNA and is not suitable for recognition of arbitrary RNA sequences. Furthermore, insertion of exogenous aptamer sequence has the potential to interfere with endogenous RNA functions. Analogous to CRISPR/Cas9-based recognition of DNA, programmable RNA recognition based on nucleic acid specificity alone without the need for genetic manipulation or libraries of RNA-binding proteins would greatly expand researchers’ ability to modify the mammalian transcriptome and enable transcriptome engineering.

Although the CRISPR/Cas9 system has evolved to recognize double-stranded DNA, recent in vitro work has demonstrated that programmable targeting of RNAs with Cas9 is possible by providing the PAM as part of an oligonucleotide (PAMmer) that hybridizes to the target RNA (O’Connell et al., 2014). By taking advantage of the Cas9 target search mechanism that relies on PAM sequences (Sternberg et al., 2014), a mismatched PAM sequence in the PAMmer/RNA hybrid allows exclusive targeting of RNA and not the encoding DNA. The high affinity and specificity of RNA recognition by Cas9 in cell-free extracts and the success of genome targeting with Cas9 indicate the potential of CRISPR/Cas9 to support programmable RNA targeting in living cells.

To assess the potential of Cas9 as a programmable RNA-binding protein in live cells, we used a modified sgRNA scaffold with improved expression and Cas9 association (Chen et al., 2013) with a stabilized PAMmer oligonucleotide that does not form a substrate for RNase H. We measured the degree of nuclear export of a nuclear localization signal-tagged nuclease-deficient Cas9-GFP fusion and demonstrate that the sgRNA alone is sufficient to promote nuclear export of Cas9 without influencing the abundance of the targeted mRNA or encoded protein. In order to evaluate whether RNA-targeting Cas9 (RCas9) signal patterns correspond with an established untagged RNA-labeling method, we compared distributions of RCas9 and fluorescence in situ hybridization (FISH) targeting ACTB mRNA. We observed high correlation among FISH and RCas9 signal that was dependent on the presence of a PAMmer, indicating the importance of the PAM for efficient RNA targeting. RNA trafficking and subcellular localization are critical to gene expression regulation and reaction to stimuli such as cellular stress. To address whether RCas9 allows tracking of RNA to oxidative stress-induced RNA/protein accumulations called stress granules, we measured ACTB, TFRC, and CCNA2 mRNA association with stress granules in cells subjected to sodium arsenite. Finally, we demonstrated the ability of RCas9 to track trafficking of ACTB mRNA to stress granules over time in living cells. This work establishes the ability of RCas9 to bind RNA in live cells and sets the foundation for manipulation of the transcriptome in addition to the genome by CRISPR/Cas9.

Thumbnail image of Figure 1. Opens large image

http://www.cell.com/cms/attachment/2050893021/2059121638/gr1.jpg

Figure 1

Targeting mRNA in Living Cells with RCas9

(A) Components required for RNA-targeting Cas9 (RCas9) recognition of mRNA include a nuclear localization signal-tagged nuclease-inactive Cas9 fused to a fluorescent protein such as GFP, a modified sgRNA with expression driven by the U6 polymerase III promoter, and a PAMmer composed of DNA and 2′-O-methyl RNA bases with a phosphodiester backbone. The sgRNA and PAMmer are antisense to adjacent regions of the target mRNA whose encoding DNA does not carry a PAM sequence. After formation of the RCas9/mRNA complex in the nucleus, the complex is exported to the cytoplasm.

(B) RCas9 nuclear co-export with GAPDH mRNA. The RCas9 system was delivered to U2OS cells with a sgRNA and PAMmer targeting the 3′ UTR of GAPDH or sgRNA and PAMmer targeting a sequence from λ bacteriophage that should not be present in human cells (“N/A”). Cellular nuclei are outlined with a dashed white line. Scale bars represent 5 microns.

(C) Fraction of cells with cytoplasmic RCas9 signal. Mean values ± SD (n = 50).

(D) A plasmid carrying the Renilla luciferase open reading frame with a β-globin 3′ UTR containing a target site for RCas9 and MS2 aptamer. A PEST protein degradation signal was appended to luciferase to reveal any translational effects of RCas9 binding to the mRNA.

(E) RNA immunoprecipitation of EGFP after transient transfection of the RCas9 system in HEK293T cells targeting the luciferase mRNA compared to non-targeting sgRNA and PAMmer or EGFP alone. Mean values ± SD (n = 3).

(F and G) Renilla luciferase mRNA (F) and protein (G) abundances were compared among the targeting and non-targeting conditions. Mean values ± SD (n = 4).

p values are calculated by Student’s t test, and one, two, and three asterisks represent p values less than 0.05, 0.01, and 0.001, respectively. See also Figure S1.

Correlation of RNA-Targeting Cas9 Signal Distributions with an Established Untagged RNA Localization Measurement

 Tracking RNA Trafficking to Stress Granules over Time
Effective RNA recognition by Cas9 in living cells while avoiding perturbation of the target transcript relies on careful design of the PAMmer and delivery of Cas9 and its cognate guide RNA to the appropriate cellular compartments. Binding of Cas9 to nucleic acids requires two critical features: a PAM DNA sequence and an adjacent spacer sequence antisense to the Cas9-associated sgRNA. By separating the PAM and sgRNA target among two molecules (the PAMmer oligonucleotide and the target mRNA) that only associate in the presence of a target mRNA, RCas9 allows recognition of RNA while avoiding the encoding DNA. To avoid unwanted degradation of the target RNA, the PAMmer is composed of a mixed 2′OMe RNA and DNA that does not form a substrate for RNase H. Further, the sgRNA features a modified scaffold that removes partial transcription termination sequences and a modified structure that promotes association with Cas9 (Chen et al., 2013). Other CRISPR/Cas systems have demonstrated RNA binding in bacteria (Hale et al., 2009, Sampson et al., 2013) or eukaryotes (Price et al., 2015), although these systems cannot discriminate RNA from DNA targets, feature RNA-targeting rules that remain unclear, or rely on large protein complexes that may be difficult to reconstitute in mammalian cells.

In this work, we demonstrate RCas9-based recognition of GAPDH, ACTB,CCNA2, and TFRC mRNAs in live cells. Because the U6-driven sgRNA is largely restricted to the nucleus, the NLS-tagged dCas9 allows association with its sgRNA and subsequent interaction with the target mRNA before nuclear co-export with the target mRNA. As an initial experiment, we evaluated the potential of RNA recognition with Cas9 by targeting GAPDH mRNA and evaluating degree of nuclear export of dCas9-mCherry (Figure 1B). Robust cytoplasmic localization of dCas9-mCherry in the presence of a sgRNA-targeting GAPDH mRNA compared to nuclear retention in the presence of a non-targeting sgRNA indicated that Cas9 association with the mRNA was sufficiently stable to support co-export from the nucleus.

RCas9 as an RNA-imaging reagent requires that RNA recognition by RCas9 does not interfere with normal RNA metabolism. Here, we show that RCas9 binding within the 3′ UTR of Renilla luciferase does not affect its mRNA abundance and translation (Figures 1F and 1G). The utility of RCas9 for imaging and other applications hinges on the recognition of endogenous transcripts, so we evaluated the influence of RCas9 targeting on GAPDH and ACTB mRNAs and observed no significant differences among the mRNA and protein abundances by western blot analysis and qRT-PCR (Figure S1). These results indicate that RCas9 targeting these 3′ UTRs does not perturb the levels of mRNA or encoded protein.

We also evaluated the ability of RCas9 to reveal RNA localization by comparing RCas9 signal patterns to FISH. We utilized a FISH probe set composed of tens of singly labeled probes targeting ACTB mRNA and compared FISH signal distributions to a single dCas9-GFP/sgRNA/PAMmer that recognizes the ACTBmRNA. Our findings indicate that the sgRNA primarily determines the degree of overlap among the FISH and RCas9 signals whereas the PAMmer plays a significant but secondary role. Importantly, in contrast to other untagged RNA localization determination methods such as FISH and molecular beacons, RCas9 is compatible with tracking untagged RNA localization in living cells and can be delivered rapidly to cells using established transfection methods. We also note that the distribution of ACTB mRNA was visualized using a single EGFP tag per transcript, and higher-sensitivity RNA tracking or single endogenous RNA molecule visualization may be possible in the future with RCas9 targeting multiple sites in a transcript or with a multiply tagged dCas9 protein.

Stress granules are translationally silent mRNA and protein accumulations that form in response to cellular stress and are increasingly thought to be involved with neurodegeneration (Li et al., 2013b). There are limited means that can track the movement of endogenous RNA to these structures in live cells (Bertrand et al., 1998). In addition to ACTB mRNA, we demonstrate that RCas9 is capable of measuring association of CCNA2 and TFRC mRNA trafficking to stress granules (Figure 3A). Upon stress induction with sodium arsenite, we observed that 50%, 39%, and 23% of stress granules featured overlapping RCas9 foci when targeting ACTB, TFRC, and CCNA2 mRNAs, respectively (Figure 3C). This result correlates with the expression levels of these transcripts (Figure S3) asACTB is expressed about 8 and 11 times more highly than CCNA2 and TFRC, respectively. We also observed that RCas9 is capable of tracking RNA localization over time as ACTB mRNA is trafficked to stress granules over a period of 30 min (Figure 3B). We noted a dependence of RCas9 signal accumulation in stress granules on stressor concentration (Figure 3D). This approach for live-cell RNA tracking stands in contrast to molecular beacons and aptamer-based RNA-tracking methods, which suffer from delivery issues and/or require alteration of the target RNA sequence via incorporation of RNA tags.

Future applications of RCas9 could allow the measurement or alteration of RNA splicing via recruitment of split fluorescent proteins or splicing factors adjacent to alternatively spliced exons. Further, the nucleic-acid-programmable nature of RCas9 lends itself to multiplexed targeting (Cong et al., 2013) and the use of Cas9 proteins that bind orthogonal sgRNAs (Esvelt et al., 2013) could support distinct activities on multiple target RNAs simultaneously. It is possible that the simple RNA targeting afforded by RCas9 could support the development of sensors that recognize specific healthy or disease-related gene expression patterns and reprogram cell behavior via alteration of gene expression or concatenation of enzymes on a target RNA (Delebecque et al., 2011, Sachdeva et al., 2014). Efforts toward Cas9 delivery in vivo are underway (Dow et al., 2015,Swiech et al., 2015, Zuris et al., 2015), and these efforts combined with existing oligonucleotide chemistries (Bennett and Swayze, 2010) could support in vivo delivery of the RCas9 system for targeted modulation of many features of RNA processing in living organisms.

RNA is subject to processing steps that include alternative splicing, nuclear export, subcellular transport, and base or backbone modifications that work in concert to regulate gene expression. The development of a programmable means of RNA recognition in order to measure and manipulate these processes has been sought after in biotechnology for decades. This work is, to our knowledge, the first demonstration of nucleic-acid-programmed RNA recognition in living cells with CRISPR/Cas9. By relying upon a sgRNA and PAMmer to determine target specificity, RCas9 supports versatile and unambiguous RNA recognition analogous to DNA recognition afforded by CRISPR/Cas9. The diverse applications supported by DNA-targeted CRISPR/Cas9 range from directed cleavage, imaging, transcription modulation, and targeted methylation, indicating the utility of both the native nucleolytic activity of Cas9 as well as the range of activities supported by Cas9-fused effectors. In addition to providing a flexible means to track this RNA in live cells, future developments of RCas9 could include effectors that modulate a variety of RNA-processing steps with applications in synthetic biology and disease modeling or treatment.

Study Unlocks Multiple Functions of CRISPR/Cas9 by Varying Guide RNAs

https://www.genomeweb.com/genetic-research/study-unlocks-multiple-functions-crisprcas9-varying-guide-rnas

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